Evaluation of Visual Function
Michael H. Sims,
Responses to Visual Stimulation
When electromagnetic waves in the range of visable light enter the eye,
the result is an alteration of electrical potentials in millions of
retinal cells. These electrical changes are propagated through several
layers of the retina and then on to the visual cortex via the optic
nerve, optic tract, and thalamus. Once in the visual cortex, these impulses
recreate the visual scene, and with the involvement of selected visual
association areas result in conscious perception. An assessment of vision
in animals without the use of verbal communication is difficult at best.
This is further complicated by an animal's ability to adapt to lose
of vision, even to the extent that its owner may be unaware of its disability.
An animal's adaptation to partial or complete loss of vision is species
dependent and related to its ability to compensate by increased reliance
on auditory and tactile sensations. What an animal can see, i.e., its
conscious awareness of visual stimulation, is not always the immediate
focus of a clinical assessment. The goal is sometimes predicting what
the animal "should" be able to see given the functional status of component
parts of the visual pathway. An animal's response to menace testing,
maze testing, and the cotton-ball test as described elsewhere are integral
parts of the visual exam. The results of these procedures and the owner's
history may still be the best estimate of what the animal can actually
Evaluation of Vision
Unlike behavioral evaluations of vision, electrodiagnostic assessments
are based on objective analyses of changes in electrical potentials
in various parts of the visual system. Therefore, none of the electrodiagnostic
procedures should be thought of as being measures of vision per se.
The primary pathway for conscious vision consists of receptor cells
(rods and cones), bipolar cells, ganglion cells, and cells in the lateral
geniculate body, and the visual cortex. The receptor and bipolar cells
are neurons that are totally contained within the retina whereas the
axons of the ganglion cells exit the eye and comprise the optic nerve
and optic tract. Each of these components and others are directly or
indirectly evaluated by electrodiagnostic tests. The responses obtained,
however, are dependent upon the type of visual stimulation, the condition
of light adaptation, type and frequency bandwidth of the amplifier,
the time window for display, and the use of signal averaging. Multichannel
recorders even allow different types of responses to be recorded simultaneously
as long as the time window is the same.
This chapter is
concerned with a general description of electrodiagnostic procedures
and their application in clinical visual testing. Some of the procedures
have not been proven to be as useful in Veterinary Medicine as others.
The electroretinogram (ERG), for example, is still the most widely reported
procedure in the veterinary literature. It is used quite often for the
diagnosis of retinal diseases such as progressive retinal atrophy (PRA)
and for an evaluation of general retinal function prior to cataract
surgery. Among the other procedures that are available are the visual
evoked potential (VEP), the pattern electroretinogram (PERG), and oscillatory
potentials (OP). These potentials have received less attention than
the ERG, but certainly could offer additional information about retinal
function in animals that might otherwise be missing from clinical evaluations.
The overwhelming majority of the veterinary literature in clinical electrodiagnosis
is concerned with dogs and less to cats, large animals and exotic animals.
As early as the middle of the nineteenth century, researchers showed
that the vertebrate eye responded to light with electrical changes and
that the retina was the source of these new potentials. The ERG is an
intricate and complex response initiated by light-sensitive cells in
the retina. The ERG is both multiphasic and transient but unfortunately
not all of its subcomponents are apparent with a single stimulus protocol.
Although the precise nature of the ERG continues to unfold with further
research, it provides a unique assessment of receptor and early central
nervous system components. The unique aspect of the ERG is that it assesses
function in structures that can also be directly visualized with an
ophthalmoscope, a privilege not possible with other electrodiagnostic
techniques. In dogs, the ERG has been useful in the diagnosis or evaluation
of retinal function in cases of cataracts, glaucoma, hemeralopia, retinal
dysplasia, toxicology screening, degenerative retinopathies, optic nerve
hypoplasia, sudden acquired retinal degeneration, or cortical blindness.2-13
The ERG can be used in cats to diagnose diseases of the retina such
as hereditary retinal degeneration14, non-inflammatory retinophathy15,
and central retinal degeneration due to dietary taurine deficiency16.
For some retinal diseases, the ERG provides a much earlier diagnosis
than an ophthalmoscopic or behavioral exam and even provides a characterization
of the function of specific cell types in the retina.
In its simplest
form, (Fig. 1) the typical vertebrate ERG consists of a early small
corneal negative potential that occurs within 10-12 msec after a bright
light stimulus. The cornea then becomes more intensely positive only
to be followed by a slower negative trough. After a period of several
hundred milliseconds, the cornea once again becomes positive. The one
negative and two positive peaks were named the a-, b-, and c-, waves,
respectively, by Eithoven and Jolly in 1908.17 The A, B, and C waves
of the ERG, which originally referred to "substances" in the eye and
the potentials they produced, are still used to refer to the three peaks
of the ERG.18
A typical canine
ERG, which was recorded by a contact lens electrode referenced to a
needle electrode inserted subcutaneously just posterior to the lateral
canthus, is shown in Figure 2. The stimulus was a white stroboscopic
flash delivered to a dog that had been dark-adapted for approximately
5 minutes. The same stimulus presented to a light-adapted dog is shown
in Figure 3.
Unless special provisions
are made in the recording technique, the ERG can be thought of as various
combinations of rod and cone responses to light. The a-wave is unquestionably
caused by photoreceptor potentials. Although the origin of the b-wave
may be open to some question, it is generally accepted that it is generated
by Muller cells. Current source density analysis and intracellular recording
electrodes support the hypothsis of radial current flow through Muller
cells. Exactly how Muller cells produce the b-wave is explained by the
movement of potassium into and out of certain portions of the cell.
It seems that light stimulation of the retina results in an increase
in extracellular potassium in both the inner and outer plexiform layers
which then promotes an influx of potassium into the portions of the
Muller cells in those layers. The potassium influx results in depolarization
of the cells and a radial current flow within the cell. The return current
through the extracellular fluid, especially in the outer layers, provides
much of the b-wave. Apparently, depolarizing bipolar cells are the source
for the potassium in the outer layers. These currents promote a vitreal-positive
potential that accounts for the polarity of the b-wave. Thus, the b-wave
is directly related to Muller cell activity and indirectly related to
activity in bipolar cells. It is interesting to note that occlusion
of the central retinal artery abolishes the b-wave but spares the photo
In most protocols
used in veterinary ophthalmology, the c-wave (also called the late positive
potential or PI) is not apparent. The c-wave has been defined as the
positive potential after the b-wave with a latency or implicit time
greater than 500 msec.19 The c-wave may be studied by using longer and
more intense stimuli and a DC-coupled amplifier (bandwidth = DC-1000
Hz). The c-wave is unusual because its implicit time increases as the
stimulus intensity increases, and because it only occurs in about one-third
of adult dogs.19 The c-wave has not been reported to be characteristically
altered in disease states in most veterinary publications.
One might reasonably
conceptualize the ERG as a number of different physiologic potentials
involving different cell types, but sharing the same time domain. Granit's
graphic separation of the "retinal action potential" into the PIII,
PII, and PI processes illustrated the relationships of the c-, b-, and
a-waves, respectively, in time.20-21 This analysis continues to command
both historic and fundamental physiologic interests. Granit's analysis
was based on a variety of experiments, one of which involved the effects
of ether on the waveform of the ERG. For both a bright stimulus and
a dim stimulus, the ERG was a composite of three independent waveforms
referred to as PI, PII, and PIII. These potentials roughly correspond
to the a-, b-, and c-wave, respectively. The order of disappearance
in response to ether administration was from PI to PII. Once PIII disappeared,
the ERG was incapable of recovery.
Light that enters
the eye may be light that participates in the formation of an image,
or it may be stray light.22 This is important to remember because the
amplitude of the ERG may or may not relate to the visual image quite
the way that some may think. One might mistakenly assume that an ERG
with a large amplitude is a "good" ERG in that it is evidence of good
retinal function. While this is generally true, an ERG elicited by an
intense stroboscopic flash may be good because many cells in the retina
are being stimulated via stray light and not because there is a good
image being formed on the retina. The physiologic difference between
stray light and image light may actually complicate the recorded response
because these two types of light cause additional peaks as a result
of differences in their respective latencies.
The clinical ERG
is usually reported by providing values for the implicit times (or latencies)
and amplitudes for the a- and b-waves. In the broadest sense, a latency
is a period of time between any two events of interest. However, the
terms implicit time have been used to refer to the time between stimulus
onset and the peak of a wave of interest. The amplitude of the a-wave
is measured from the prestimulus baseline to the nadir of the peak and
the b-wave is measured from the nadir of the a-wave to the peak of the
b-wave. The effects of retinal lesions on the amplitude or implicit
time of the ERG are somewhat predictable. A retinopathy, which involves
large areas of the retina will result in decreased amplitudes and prolonged
implicit times, whereas focal lesions may result in decreased amplitudes,
but the implicit times are not altered.23
in the retina may be recorded during the same period of time that is
occupied by the ERG. These include a differentiation of the a- and b-waves
into photopic and scotopic components, the early receptor component
(ERP), the scotopic response threshold (STR), oscillatory potentials
(OP), the late negative potential, and the d-wave. Some of these activities
are apparent when the visual stimulus is presented in a special way,
and others have more to do with how the activity is recorded or the
preparation and/or the light adaptation of the animal. In animals such
as dogs that have high concentrations of rods in their retinas, the
c-wave may show a negative off deflection if the stimulus has a long
Recording the Flash Electroretinogram.
The flash ERG, or FERG, is a mass response of the retina to full-field
stimulation of the retina with a flash of light. Like other modern electrodiagnostic
procedures, electroretinography can involve advanced techniques and
sophisticated recording equipment that one might expect to find in a
specialty practice or veterinary teaching hospital, or it can be a very
simple procedure that can be recorded with uncomplicated instruments.
A simple strobe light capable of triggering an oscilloscope equipped
with good physiologic amplifiers that can provide low-noise amplification
in the range of 104 will provide valuable information about visual function.
If the clinician is attempting to assess the integrity of the retina
prior to cataract surgery, an ERG can be reported as pass/fail based
on previously established criteria. However, if there is an attempt
to gather objective data for diagnosing specific retinal diseases, or
for following the course of a disease through serial examinations, then
the protocol and the equipment should be more sophisticated.24
Electrodes. The recording electrode may be one of several different
types including contact lens, cotton wick, gold foil, and subdermal
needle electrodes. The primary considerations in the selection of electrodes
are accuracy and reliability, cost, potential of trauma to the patient,
fit, and ease of use. Most commercially available electrodes are made
of silver, gold, or platnium, but they can also be constructed from
38 AWG teflon-insulated stainless steel wire25 or silver-impregnated
microfibers.26 Contact lens electrodes are probably used more often
than any other because they are non-traumatic and provide reliable and
reproducable results. With contact lens electrodes, an ionic medium
such as hydroxyproply methylcellulose solution, is used to insure good
electrical contact between the electrode and the cornea. Needle electrodes
have been used in animals, but ERGs recorded with contact lens electrodes
have significantly greater amplitudes than those recorded with subdermal
potentials are small (usually 1 mV or less) and in order for them to
be properly visualized, a system of preamplifiers and amplifiers are
necessary. The three inputs (positive, negative and ground) are connected
to a high quality differential amplifier so that a positive potential
occuring at the active electrode results in an upward deflection in
the response. The amplifier should have band-pass filters that allows
an attenuation of frequencies below and above the low and high settings,
respectively. The bandwidth of the amplifier may vary, depending on
the purpose of the procedure. For ERGs, some have used a bandwidth as
narrow as 0.8-250 Hz29, While others have used wider bandwidths such
as 1-3000 Hz9. Using a bandwidth of DC-1000 Hz will permit a recording
of the c-wave19. The choice of bandwidths is dependent upon which visual
potential is being analyzed. Suggested bandwidths for visual potentials
are as follows: electro-oculogram (dc-100 Hz); ERG a- and b-waves (0.2-200
Hz); oscillatory potentials (90-300 Hz); ERG c-wave (dc-200 Hz); pattern
ERG (0.1-200 Hz); visual evoked potentials (1-300 Hz).30
Many of the commercially
available electrodiagnostic systems include analog-to-digital converters
early in the stages of amplification. A response converted to a digital
format then allows for ease of storage and subsequent analysis with
a variety of computer programs.
photostimulator such as a xenon flash tube provides short-duration flashes
of light to the light- or dark-adapted eye and is probably the most
popular light source for clinical testing. The strobe is small and simple
to use, but the disadvantages include difficulty in calibration, variation
in output, and electromagnetic artifacts. The Tungsten/Quartz/Halogen
light source, as a part of an optical stimulator, is more exactly calibrated,
and can give repeatable stimulation for longer periods of time, but
is much larger and more complicated to construct. Strobe units are usually
placed 20-30 cm from the test eye whereas a fiber optic light guide
can be used to deliver light from a tungsten halide lamp.31 The intensity
of the stimulus will vary greatly with the type of flash used, but it
is recommended that a minimum intensity of at least 4.0 log units greater
than the absolute dark adapted threshold be used. This will mean that
the stimulus is only 80-90% of that required for saturation2. Ganzfeld
stimulators have also been used successfully in dogs, and provide indirect
and homogeneous illumination of the visual field.32 This device also
provides adapting background illumination in addition to stroboscopic
flashes of light.
Signal averagers may be used to enhance the signal-to-noise ratio
of a response33-34. A signal averager is basically a computer that stores
voltage values in bins at fixed times after the stimulus application.
After the next stimulus application, the new voltage in each bin is
added to the previous voltage and the sum divided by two. This process
is repeated for a predetermined number of stimuli and the result is
an averaged response that will look more or less like any single trace
depending on the amount of background noise. This technique is particularly
helpful when anesthesia is not in the best interest of the patient and
some movement must be tolerated. The most common source of physiologic
noise is muscle activity from the eyelids, which is enhanced if these
muscles are stretched with a speculum. Signal averagers reduce electromyographic
noise because this type of activity is truly random with respect to
the stimulus trigger. In some instances, noise is the result of a faulty
protocol and lengthy averaging is certainly not a an acceptable remedy.
Recording ERGs from awake human beings or animals is not a painful
process, but the procedure does require cooperation on the part of the
patient. Because this level of cooperation is usually not attainable
in conscious animals, anesthesia is often used to prevent movement artifacts,
reduce patient stress, and allows the examiner to fix the position of
the eye relative to the light source and recording electrodes. Most
clinical protocols for anesthetized animals are designed to produce
minimal effects that are then incorporated into a baseline. The most
common effect of anesthesia on the ERG in dogs is general depression,
i.e., a reduction in amplitude and an increase in implicit times.35
The effects of gaseous anesthetics, such as halothane2 or isoflurane,9
have some effect on the ERG, but this is offset by the elimination of
much larger more consequential artifacts.2 To unequivocally demonstrate
the specific effects of anesthetic agents in animals would require data
before and after drug administration to be equally free of artifacts.
This was accomplished in a study in dogs by comparing ERGs recorded
under halothane anesthesia to ERGs recorded under succinylcholine akinesia.36
There were differences in most recorded variables with the most notable
being a 36-77% reduction in the b-wave amplitude. In most ERGs under
halothane, the latencies were prolonged with the exception of the dark-adapted
series. It was further reported that the halothane-induced changes were
independent of light and dark adaptation and independent of cone- and
rod-mediated responses. The overall effects of halothane may simply
be related to its ability to interfere with membrane transport.36 An
anesthetic protocol that has given good results in dogs is the use of
sodium thiopentone and halothane.37 An isoflurane-nitrous oxide protocol
has been used in dogs because of its low glood:gas partition coefficent
for rapid induction, low biotransformation, decreased myocardial sensitivity
to catecholamines and positive tidal volume trend.9
Protocols for recording
ERG in awake and freely moving animals have been developed38-39, but
they are not ideal for clinical evaluations. Although signal averaging
can appear to reduce artifacts encountered when recording from awake
animals, this is probably not the best alternative. In rhesus monkeys,
cone adaptation curves (response to 40-Hz flicker) were used to assess
the influence of inhalant anesthetics on the ERG during the course of
dark adaptation.40 The volatile anesthetics that were tested were methoxyflurane,
halothane, enflurane, ether, and choloroform. All of the agents were
shown to retard dark adaptation, perhaps by reducing the rate of photopigment
regeneration. The ERG in rabbits was used to test for the effects of
the volatile anesthetics methoxyflurane, halothane, and enflurane.41
The amplitudes of the a-wave and OP peak O1 showed dose-dependent decreases
in amplitude. Even more striking were the change in O1 latencies. Also
in rabbits, it was shown that alpha blockers reduced ERG amplitudes
and beta agonists increased the retinal response to blue, red and white
light. Adrenalin revealed mixed responses.42 Urethane anesthesia did
not have an effect on the ERGs in mice, but dopamine blockade using
haloperidol reduced the amplitude. However, that may have been due to
a slight toxic retinitis in the inner retinal layer.43 A study in rats
revealed that rod saturation is anesthetic dependent when comparing
urethrane and pentobarbitol.44
of ketamine and xylazine in dogs was reported to be preferable to thiopentane,
halothane and nitrous oxide.45 Thirty one ophthalmascopically normal
Labrador Retrievers that were given varying dosages of xylazine and
ketamine did not show any significant changes in the ERG elicited by
single flashes that were 1.60 log relative units above b-wave threshold.46
The dosages of xylazine ranged from 0.96-1.23 mg/kg body weight IM and
ketamine ranged from 7.8-10.1 mg/kg body weight, IM. The addition of
acepromazine (0.5 mg/kg IV) to ketamine hydrochloride (10 mg/kg IM)
was reported to provide good immobilization in dogs for electroretinography.7
In another study, a combination of glycopyrrolate (0.01 mg/kg) and medetomidine
hjydrochloride (15 ug/kg), was given IM to dogs. Twenty minutes later,
ketamine hydrochloride (10 mg/kg) was given IV followed by vicuroniuim
bromide (0.2 mg/kg) IV. This anesthetic regime, which was designed to
prevent interference with receptor hyperpolarization during stimulation
and to provide adequeate anesthesia and muscle relaxation, provided
the 10-12 minutes necessary for an ERG exam.
In a recent study,
dogs were sedated with IV ketamine (5 mg/kg) and then given 40 ug/kg
of vecuronium bromide. Throughout the recording period, anesthesia was
maintained with 25% oxygen and 75% nitrous oxide and muscle paralysis
was sustained with vecuronium bromide at a rate of 400 ug/kg/hr.47 A
similar procedure consisted of glycopyrrolate (0.01 mg/kg, IM), induction
with thiamylal sodium (15 mg/kg, IV), and after incubation, pancuronium
bromide (0.1 mg/kg, IV) to promote muscle relaxation.19 General anesthesia
in cats undergoing electroretinographic examination has been achieved
with sodium thiopentone and maintained with halothane14 or a mixture
of ketamine hydrochloride (25 mg/kg, IM) and xylazine HCl (2.5 mg/kg,
IM).48 One of the potential consequences of anesthesia is a depression
of respiratory activity and possibly hypoxia. At a PaO2 of 45 mm Hg,
the ERG begins to show the effects of hypoxia. The b-wave is affected
first as seen in a decrease of the amplitude and an increase in the
latency.8 The a-wave is apparently more resistent to decreased oxygen
tension and remains after the b-wave is extinguished. The same trend
is true when perfusion pressure is decreased. In experiments designed
to look at c-wave changes in the face of increasing intraocular pressure
(IOP) and decreased choroidalal oxygen tensions, it was observed that
the ERG b-wave was less sensitive to changes than the c-wave.49 It was
hypothesized that increasing IOP decreased choroidal blood flow which
caused hypoxia and early changes in the c-wave, primarily an increase
in amplitude. This may have been due to the inability of the choroidal
circulation to autoregulate the way the retinal circulation does. In
addition to the direct effects of anesthetic agents or hypoxia, the
ERG in dogs has been shown to be adversely affected by CO2. Hyperventilation
in anesthetized dogs enhanced the b-wave, and it was proposed that the
mechanism was the reduction of CO2.50
Separation of Rod and Cone Function
The ERG provides clinicians with the opportunity of examining not
only the retina in general, but also specific classes of photoreceptors.
It should be the aim of any clinical protocol for recording ERGs to
include a method for separating rod and cone components in the recordings.
This is achieved primarily by varying the wavelength, intensity, duration,
and position of light on the retina and by the frequency of stimulations.
Manipulation of these variables allows one to take advantage of the
characteristic ways that rods and cones respond to different types of
light stimulation at different levels of light or dark adaptation as
described in the duplicity theory. This theory states that the retina
is characterized by two active systems, one that is based on rod function
and one based on cone function. It has become common practice to refer
to rod and cone systems as scotopic and photopic, respectively. Actually,
the terms scotopic and photopic refer to the ambient light conditions
during the test, i.e., a scotopic ERG is one recorded in the dark and
a photopic ERG is one recorded in the light. Rods and cones contribute
their signals to the ERG independently of each other and under certain
conditions, their activities can be separated. Cones respond best to
more intense light in the longer (red) wavelengths and can discharge
at a more rapid rate, whereas rods respond best to shorter (blue) wavelengths
at lower intensities and lower rates of discharge. Red flashes are produced
by placing Kodak Wratten filter 25 in front of white light and blue
flashes are produced by using Kokak Wratten filters 47, 47A, and 47B.
Cones maintain sensitivity in the presence of background illumination
whereas rod sensitivity decreases. A stimulus may activate both systems
simultaneously or accentuate one or the other system. The exact nature
of the response may also depend on the area of the retina that is stimulated.
Cones are more numerous in the area centralis whereas rods increase
in the peripheral zones in the retina.51
Some clinical electrodiagnosticians
have proposed five ERG responses to be recorded as a minimum standard
1) a mixed rod and cone response obtained by a high intensity stimulus
in a dark adapted eye,
2) a rod response by using a low intensity stimulus in a dark-adapted
3) oscillatory potentials elicited by a high intensity stimulus in a
4) cone response by high intensity stimulus in the light adapted eye
( or other techniques), and
5) responses obtained by a rapidly repeated stimulus (flicker).52
The length of time that an animal has been dark-adapted can also be
used to further accentuate rod/cone separation. During the early phase
of dark adaptation, a red flash can be used to demonstrate cone function.
The development of the photopic b-wave occurs first with a low amplitude
and short implicit time.53 This even occurs in animals such as owls,
in which the retina is a predominantly populated with rods.54 As dark
adaptation continues, however, the scotopic b-wave masks the photopic
b-wave with its greater amplitude and longer implicit time. This sequential
masking of the photopic b-wave with a scotopic b-wave does not occur
in all animals. In sheep,55 deer,56 and swine,57 the photopic (bp) and
scotopic (bs) b waves can be seen together as different peaks during
A rapid rate of light stimulation, or flicker, can also be used to separate
rod and cone function. Flicker fusion is the frequency of stimulation
at which individual responses can no longer be discerned. A bipartite
flicker fusion response curve (FFRC) is a graph in which the log-luminance
of the stimulus is plotted against the maximum frequency (flashes/sec)
at which individual responses occur. The curve is characteristic for
most dark-adapted mammals in that there is both a rod slope and a cone
slope (Fig. 4). The shallow portion of the curve represents rod fusion
at low frequencies and low intensity stimulation whereas the steeper
portion of the curve represents cone fusion at greater intensities.
The FFRC for the dark-adapted dog is similar to that recorded in human
beings except for slight shifts along the log-luminance axis.58 The
electrical activity from cones can be selectively recorded because only
cones are able to keep pace with a flash rate of 30/sec.
has also been used to examine the photopigment complements in dogs and
foxes.59 These canids were shown to have a cone pigment with a peak
sensitivity at 555 nm and a second one in the 430-435 nm range. The
rod pigment had a peak at 508 nm or in a range of 500-510 nm.47 These
results support the prediction that dichromatic color vision is characteristic
of both dogs and foxes. A similar procedure was used in squirrel monkeys
in which color-vision had been previously established using behavioral
tests.60 In 12 monkeys, three different varieties of dichromacy were
demonstrated. Prairie dogs also have two distinct photopigments but
only one morphologically distinct receptor type (cones).61
red and blue light can be used to characterize diseases that have a
predilection for receptors in one or the other system. If a long-wavelength
(red) light produces an ERG with the same amplitude as does a short-wavelength
(blue) light in a dark-adapted animal, then the stimuli are said to
be scotopically balanced. The clinical use of these stimuli can reveal
underlying causes of abnormal ERG responses resulting from monochromatic
(white) light stimulation. For example, low-amplitude ERGs elicited
by white light in dark-adapted Norwegian elkhounds was shown to consist
primarily of the cone response. Rod dysplasia in these dogs basically
eliminated the large rod response normally evoked by blue light.2
Even when red and
blue lights are balanced, rod activity may mask cone activity in the
resultant records at certain stages of dark adaptation.47 This may require
further means for isolating the smaller cone activities by the use of
a background light that eliminates rod components. This can be shown
by the use of balanced red and blue stimuli in the presence of blue-green
background light of increasing intensity. Figure 5 illustrates the similarity
of the waveform produced by scotopically balanced red and blue light
in dark-adapted dogs. Notice, however, the diminishing rod b-waves that
were evoked by both blue and red stimuli as the relative intensity of
the background light increased; the blue light no longer evoked a rod
or cone response, but the red light produced a small cone b-wave with
a short implicit time and low amplitude (left column). Furthermore,
as soon as the scoptic b-wave appears during dark adaptation, the photopic
b-wave will be masked and will no longer be apparent.
The values for ERG implicit times and amplitudes in normal animals
will vary according to the type and intensity of the flash, the type
of recording electrodes, the bandwidth of the amplifier, and the length
of time in the light or dark. Because no two labs use exactly the same
protocol, a comparison of normal values will be difficult. A high intensity
white flash presented to dogs dark-adapted for three minutes had mean
a- and b-wave implicit times of 14.3 and 36 msec, respectively and amplitudes
of 44 and 108 mV, respectively.33 The amplitudes of the a- and b-wave
increase linearly as the stimulus intensity is increased logarithmically
and as the period of dark adaptation increases up to about 60 minutes.
After 60 minutes of dark adaptation in adult dogs, scotopic ERGs had
a- and b-wave amplitudes of 99.3 and 316.7 mV, respectively,9 and a-
and b-wave implicit times of 13.6 and 34 msec, respectively. Using a
slightly different protocol that included 15 minutes of dark adaptation,
a-waves were reported to have a mean amplitude of 41.56 mV and b-waves
had a mean of 148.21 mV.62
Flash ERGs recorded
from anesthetized cats, which were dark-adapted for 60 minutes, were
characterized by an a-wave with an amplitude of 160.6 mV and an implicit
time of 13.2 msec.63 The b-wave had an amplitude of 521.5 mV and an
implicit time of 34.8 msec.
Flash ERGs recorded
from Japanese Black and Holstein-friesian cattle were used to assess
retinal function in visually deficient calves.64 After 15 minutes of
dark adaptation, the amplitudes of a-waves ranged from 573-695 mV and
the b-wave amplitudes ranged from 1,075-1,305 mV. The latencies of the
a- and b-waves ranged from 9-12 msec and 36-41 msec, respectively. In
light-adapted Holstein cows, mean a- and b-wave latencies were 13.9
and 30.2 msec, respectively and mean b-wave amplitudes were 43.24 mV.65
Threshold Response (STR)
There are several negative components that contribute to the early
phase of the cat ERG, some of which are strongly rod-dependent.66 These
include a sustained negative potential, a negative going off response,
and the M-wave. A rod-driven response in dark-adapted cats was reported
to occur in the proximal retina at a 17% depth that is clearly different
from the b-wave that occurs at a depth of 48%.67 This activity, which
is called the scotopic threshold response (STR) contributes a negative
potential to the diffuse ERG at threshold. At low stimulus intensities,
the STR may actually resemble the a-wave that occurs with more intense
stimulation.68 The STR appears to approximate the threshold of the most
sensitive ganglion cells in cats and may be caused by proximal retinal
neurons with an indirect participation by Muller cells. The contribution
of the STR to the vitreal ERG at low stimulus intensities closely follows
its presence in the proximal retina.
The SRT in the canine
is a corneal negative response elicited by dim light stimulation even
below that required for the scotopic b-wave (Fig. 6).69 This response,
with amplitudes as high as 120 mV and implicit times that range from
75-96 msec, has a spectral sensitivity of that corresponding to the
canine rod visual pigment. Further evidence of the scotopic nature of
this response is evidenced by its disappearance in the presence of a
dim background light that has no effect on the a- and b-wave components.
Much of the research devoted to identifying the structural contributors
to the ERG has been based on those responses elicited by flashes of
light. The flash stimulus produces a distinct response and as presented
earlier, many refer to the flash ERG as the FERG. Cortical neurons are
known to be rather insensitive to homogeneous light stimulation and
there is reason to believe that patterned stimulation excites different
retinal cells than non-patterned stimulation. The pattern-evoked electroretinogram
or PERG is a type of ERG elicited by phase-reversal gratings.70 The
pattern consists of checks or bars that are periodically reversed such
that the light areas become dark and vice versa. In this way, the overall
mean luminance remains constant and the stimulus is characterized by
overall brightness, contrast between light and dark areas, the size
of the gratings, and the rate of reversal. A further condition of this
procedure requires that the stimulus be focused and stable on the retina.
Accurate refraction and patient cooperation are essential but the response
permits an examination of pattern-processing functions of the retina.
The source of the
PERG is retinal, but different from the uniform-field FERG. Unlike the
FERG, which is influenced by the luminance of the stimulus, the PERG
relates more to the pattern of the stimulus and is dependent upon bandpass
spatial characteristics. That is, the response is highly influenced
by size of the pattern elements in such a way that increasing or decreasing
spatial resolution increases or decreases components of the PERG. The
PERG has been useful in human beings for the clinical diagnosis of retinal
ischemia, macular disorders, optic nerve dysfunction, glaucoma, diabetes,
amblyopia, Alzheimer's disease, increased intraocular pressure, and
difference between PERG and FERG is that only the former is significantly
suppressed by degeneration of ganglion cell axons.72-73 Several weeks
after the optic nerve was transsected in cats, the amplitude of the
PERG decreased while the amplitude of the FERG remained constant. Because
the reduction in PERG amplitude paralleled the degeneration of ganglion
cells, it was concluded that the source of response was in the inner
layers of the retina. While in primates, the PERG is predominantly photopic,
it is not surprising that the PERG is a mixed response in cats.74 The
PERG has been used in dogs75-76 and cats77 to assess the limits of visual
resolution. When similar techniques are performed in human beings, the
correlation between the PERG estimate of resolution and verbal communication
of visual resolution is significant.
The PERG has also
been used in dogs to assess primary open angle glaucoma (POAG).76 The
dogs tested were those with moderate signs of glaucoma including open
iridocorneal angles, elevated intraocular pressure, cupping of the optic
disc and disentergration of zonular ligaments. The visual resolution
of the central 15° of the retina in normal dogs was 6.9 +2.6 minutes
of arc/phase whereas the resolution in the toroidal 15° was 11.8+2.3
minutes of arc/phase. There were no significant differences between
the normal and the glaucomatous dogs. Apparently, young dogs do not
experience loss of visual resolution in the early stages of glaucoma.
Using this procedure, the visual resolution in dogs is greater than
that in cats, which correlates with a greater number of ganglion cells
and optic nerve fibers.76
PERG have been reported
in dogs using square-wave vertical grating patterns presented at spatial
frequencies ranging from 0.015-1.92 cyles/degree.78 Signal averaging
of responses elicited by low spatial frequencies produced a PERG characterized
by a small negative peak (N1), a large positive peak (P1), and a much
larger negative peak (N2) (Fig. 7). Increases in spatial frequencies
caused a decrease in the amplitudes of P1 and N2 and an increase in
the peak times of N1 and P1. PERG have been recorded in cats and unlike
those recorded from human beings and dogs do not show a b-wave.79 The
feline PERG consisted primarily of a vitreous negative after potential
peaking about 120-200 msec after pattern reversal. The response amplitudes
decreased with increasing spatial frequency and showed low-frequency
attenuation with sinusoidal phase reversal but not with square wave
reversal. This observation is important in identifying a pattern-specific
component involving lateral interactions in the retina.
Superimposed on the a- and b-waves of the ERG are four to ten peaks
or wavelets collectively referred to as oscillatory potentials (OP).
Oscillatory potentials have been reported in several animal species80-81
including dogs,82-83 and cats63-84. Although the name may imply a periodic
activity, the OP are probably not true reverberations. The ERG and OP
occur during the same time period but they represent different physiologic
activities and have different cellular generators. Because OP are smaller
than the ERG in which they are embedded, special recording procedures
are used to better visualize the individual components.63, 82, 85
Direct retinal recordings
and the use of pharmacologic agents that specifically interfere with
selected cellular components have provided further information about
OP. Intraretinal depth recordings of OP reveal that they probably arise
from the interplexiform layer of the retina distal to ganglion cells
and proximal to receptor cells.86 Furthermore, OP appear to represent
a radial current flow involving inhibitory feedback circuits that are
initiated by amacrine cells87 and each peak probably has a different
origin.88 A recent report has provided evidence that the renin-angiotensin
system has a direct effect on retinal neurons that is not related to
its systemic effects.89 Such evidence supports the hypothesis of an
antiotensinergic process involving amacrine cells in the inner retina.
Reserpine, caused a selective suppression of later OP components in
cats without a significant change in the a- or b-waves or early OP components.90
These observations appear to indicate a definite link between the activity
of dopaminergic cells and generation of at least some of the OP peaks.87
Although the cones have been favored as generators of OP, some investigators
have reported that both rods and cones participate.85
Like the ERG, characteristics
of OP depend upon the intensity, rate, and spectral characteristics
of the stimulus and the state of retinal adaptation. Selected aspects
of the stimulus or recording amplifier can be manipulated to accentuate
the OP and also reduce variability include bandpass filtering, dark
adaptation, stimulus conditioning, stimulus duration, and signal averaging.
The OP are best recorded with an intense white light stimulus. The dominant
frequency of OPs is in the 100-160 Hz range depending on the state of
adaptation. The OP can be selectively enhanced in dogs and cats by settting
the bandwidth of a recording amplifier to a low frequency of 100 Hz
and a high frequency of 500 Hz, (Fig. 8). Because OP are quite large
in dark adapted animals, they are also visible in ERGs recorded with
wider amplifier bandwidths (Fig. 9). Those OP peaks that occur on the
peak of the b-wave are problematic because they obscure the exact point
at which the b-wave is measured. To eliminate this, the high frequency
setting can be reduced, but this artificially prolongs the latencies
of both the a- and b-waves.91
Studies in human
beings have demonstrated what is called a conditioning flash effect
or CFE. Because the OP responses to flashes after the first of a series
are larger and less variable than those elicited by the first flash,
it is thought that the first response is somehow confounded by rod participation
and subsequent responses are basically cone responses85. This would
appear to indicate that OP are best recorded in the mesopic range of
retinal sensitivity, i.e., somewhere between scotopic and photopic conditions.
have been utilized clinically to assess several ophthalmologic disorders,
such as diabetic retinopathy, retinal ischemia, pigmentary retinal degenerations,
chloroquine retinopathy, central retinal artery occlusion, glaucoma,
Alzheimer's disease, and other diffuse chorioretinal degenerations.92-94
Because OP are dependent on good retinal circulation, acute increases
in intraocular pressure (IOP) cause changes in both latencies and amplitudes
of OP peaks in dogs. 83 A 300% increase in IOP for 3-5 minutes completely
obliterated both OP and ERG. Both responses return to normal when pressures
are reduced to baseline. In this study, there was an average increase
of 89.4% in the amplitude of OP peaks and an 81.68% increase in the
b-wave amplitude by the end of 60 minutes of dark adaptation.
The effects of stimulus
conditioning and intensity on OP peaks 01-04 were studied in anesthetized
cats.63 In this study, there were mean decreases in peak time that ranged
from 17.81 to 29.47 msec and mean amplitude increases of 19.72 to 57.03
lV for peaks O1-O4 across 3 log units of stimulus increase. Clearly
then, OP peak time and amplitude should be considered as functions of
stimulus intensity. The curves for peak time and amplitude reveal a
distinct difference between O1 and O2-O4; one that is more dramatic
for amplitude than peak time. This supports the claims of others that
OP peaks probably have different generators. Studies have emphazised
the uniqueness of O4 in humans, but the present study in cats seems
to accentuate the activities of O1.
An electrodiagnostic evaluation of the visual system should include
recordings of retinal activity, but also recordings of postretinal activity.
Visual evoked potentials (VEP) are averaged postretinal potentials that
arise from areas of the brain in response to visual stimulation. Possible
generators of the VEP include rostral colliculi or their brachia, pretectal
areas, and specific cortical visual areas. The clinical rationale for
recording VEP is simple; a normal response indicates that the visual
pathways from the retina to the visual cortex are intact. The involvement
of the retina in the VEP is somewhat different from its role in the
clinical ERG. The ERG is generated by large areas of the retina, but
the VEP provides an indirect assessment of signals that originate primarily
in the area centralis. The independence of retinal and postretinal visual
potentials was recently demonstrated in a study in cats.48 Long-term
(3-4 years) monocular visual deprivation was accomplished by lid sutures.
At the end of the deprivation period, VEP were virtually eliminated
in the test eye whereas PERG and flash ERG were unaffected. Several
techniques have been described for recording VEP in dogs using a stroboscopic
white flash for visual stimulation.39, 95-101 Others use a different
type of stimulation such as LED light sources102 or square-wave vertical
gratings.75 In most of the reports, VEP were recorded from anesthetized
dogs,96-100 but some were recorded from awake dogs lightly restrained
in a body sling.101 In some of the studies, dogs were dark adapted39,
95-97 and some were light adapted.100 A canine VEP can be recorded from
subcutaneous electrodes overlying the brain in response to a flash or
pattern-reversal stimulation. An example of a VEP recorded by a positive
electrode placed subcutaneously about 3 cm. rostral to the bregma and
referenced to a negative electrode placed under the chin is shown in
Figure 10. These responses were recorded from the left side of the brain
in response to stimulation of the right eye. Light stimulation was achieved
with a 3x5 matrix of light-emitting diodes. In light-adapted cats, VEP
were characterized by a polyphasic potential with latencies in the 0-100
ms range (Fig. 11).103
In human beings,
VEP have been helpful in diagnosing demyelination, optic nerve damage
as a consequence of glaucoma, axonal neuropathy, maculopathy and neurotransmitter
deficiencies.104 Pattern-reversal stimulation is produced by a video
display connected to a pattern generator or computer. Human patients
are asked to fix the eyes at the center of the grating and maintain
a focus throughout the procedure. Contrast of a stimulus projected onto
the retina is important because of the center-surround organization
of retina cells.104 The organization of receptive fields are not uniform
across the entire retina and thus the pattern that best stimulates retinal
components may vary in different species.
In addition to its
role in disease diagnosis, the VEP has been used in humans and animals
to predict subjective psychophysical contrast sensitivity or limits
of spatial resolution.105 The differences between VEPs from different
animals are more striking than the differences between ERGs. This is
due not only the greater complexity of the VEP, but to a wider variety
of recording protocols. As with other electrodiagnostic procedures that
are not particularly painful but do require patient cooperation, VEP
are usually recorded in anesthetized animals.
The exact waveform
of the response will depend on the type and level of anesthesia, placement
of electrodes, method of stimulation, and body temperature of the animal.100
White stroboscopic flashes were used to record VEP from rats, guinea
pigs, cats, monkeys, and human beings using similar technique.106 The
responses were similar among the species and consisted of 3-4 positive
peaks with latencies ranging from 15-274 msec. Cats were particularly
noteworthy because of fast P-N components during the first 45 msec.
The interhemispheric variability in the VEP was shown to relate to the
percentage of fibers that cross the midline in the chiasma. In cats,
about 65% of the fibers in the optic nerve cross in the chiasma and
in dogs, about 75% cross.107 In response to white light flash in dogs,
VEP were characterized by a single positive peak with an average latency
of 58 msec.99 In a later study in dogs also using a white flash stimulus,
the VEP consisted of three positive peaks, P1, P2, and P3 with mean
latencies of 14.3, 54.5, and 98.1 msec, respectively (Strain et al.,
1990). In those studies that used stroboscopic flashes of white light,
caution was advised because of the likelihood of volume conducted ERGs
comprising much of the VEP activity recorded from scalp electrodes.96,
Using a 3 x 5 matrix
of light-emitting diodes as a stimulator, VEP and ERG were recorded
from 10 normal light-adapted adult dogs.103 The LED are quiet and preclude
the VEP from containing stray auditory-evoked potentials. Four scalp
electrodes were used to record VEP and ERG were recorded by 2 scalp
electrodes near the eye and by a conjunctival electrode. The VEP consisted
of 3 major positive peaks (P1 to P3) with peak latencies ranging from
20 to 70 msec (Fig. 12). There was no differences between the latencies
of peaks P1-P3 when comparing VEP recorded 1 week apart in the same
dog. The likelihood of volume-conducted activity from the retina was
thus reduced in two ways. First, because the total illuminance of the
LED matrix was much less than that of the average stroboscopic flash,
the amplitude of the ERG was substantially reduced. What little remained
of the ERG could be easily masked, even by low-amplitude cortical activity.
Second, the amplitude of the ERG was low because the VEP were recorded
from light-adapted dogs. The ERG was a low amplitude cone response.
origin of the VEP was substantiated by recording VEP before and after
unilateral optic nerve transsections in 4 dogs.102 Electroretinograms
were also measured before and after surgery to assess the integrity
of the retina. Postsurgically, the VEP was absent when the eye on the
operated side was stimulated. Stimulation of the contralateral eye produced
VEP with the same waveform shape, but the latencies were slightly prolonged
when compared to presurgical recordings. Electroretinograms recorded
from the remaining eye also had slightly prolonged b wave implicit times,
but when these times were compared to ERG from the intact eye after
surgery, there were no differences.
The VEP waveforms
in animals are usually polyphasic and consist of positive and negative
peaks in the 0-100 msec range. The nomenclature most commonly used is
a designation of "P" for positive and "N" for negative followed by a
number indicative of the order of the peak. In some cases, the number
following the peak gives the expected mean value of the latency. For
example, the P100 that is characteristic of VEP elicited by pattern-reversal
stimulation in human beings is the positive peak with a mean latency
of 100 msec. The primary clinical analysis of VEP consists of measuring
the latencies and amplitudes of resultant peaks, especially the most
prominent and/or the most stable potential. In human beings, this would
be the P100.
The VEP, together
with other tests, can provide data from different portions of the visual
pathway. The simultaneous recording of PERG and VEP could potentially
permit a differentiation of demyelinating conditions of the optic nerve
for example, and lesions causing complete axonal loss and degeneration
of ganglion cells.92 The VEP is particularly helpful in diagnosing blindness
that may be post-retinal in origin. Optic nerve hypoplasia is an inherited
disease that commonly causes blindness in dogs.109 Opthalmoscopically,
the optic nerve head is small and this is accompanied by fixed and dilated
pupils. The histopathologic changes include hypoplasia of ganglion cells
and nerve fiber layers. One would reasonably expect the ERG associated
with this condition to be normal, but the VEP is dramatically altered.
Sheep and goats with thiamine-responsive polioencephalomalacia (PEM)
were reported to have abnormal VEP but normal ERG.108 The sudden onset
of blindness in PEM is reported to be cortical as a result of neuronal
degeneration in gray matter.
Development of Visual Potentials
Electrodiagnostic procedures have become very important for the early
diagnosis of selected eye diseases in animals. Unaffected littermates
may provide age-matched controls, but data collected during the maturation
of normal animals is also needed if entire litters are affected. The
maturation of the two receptor types may differ within the same animal
and differ among species. Most animals have retinas in which both rods
and cones develop with age, even though they develop at different rates.
Exceptions to this general rule are the tree shrew (Tupaia) and some
Sciuridae, which have retinas that contain only cones.61
At birth, the photoreceptor
layer in the canine retina is not formed; i.e., the two granular layers
have not separated. The ERG is absent at birth, but begins to appear
in puppies at about 10-15 days of age and is completely formed by 15-28
days of age.62, 97, 110 The first response to occur is a small negative
wave that appears at the beginning of the a-wave. This small negative
response occurrs at the time of differentiation of the rods and cones.
During development, the amplitudes increase and latencies decrease until
they approximate adult values between the 5th and 8th weeks of age.62,
110 The greatest changes in ERG amplitude are expected to occur between
the 3rd and 4th weeks of age at a time that corresponds to maturation
of the inner and outer nuclear layers.62 Maturation is evidenced by
an increase in the amplitude of the b-wave and a decrease in the latency.
Using a stimulus equal to 4.0 log foot lamberts, the amplitudes for
a- and b-waves in three-week-old pups were on the order of 0-15 mV and
25-50 mV, respectively.7 One week later, the amplitudes had increased
to 0-90 mV and 40-135 mV, respectively. In newborn lambs, the implicit
times for a- and b-waves decreased during from birth to 30 days of age,
but the interval between the respective peaks did not change.111 This
was interpreted as meaning that the maturation was primarily occurring
in the photoreceptors.
In Red Irish Setters,
the b-wave reaches its full size between 40 and 50 days.10 High amplitude
ERGs occur during maturation at a time when the retina is reaching maturity.
In vitro recordings of transretinal mass receptor potentials in 9 to
10-week-old dogs point to potential changes across photoreceptors as
the primary cause of the amplitude increase.112 Clearly, the cone system
in dogs develops more rapidly than the rod system.113 The amplitudes
of the ERG components increase and the implicit times decrease with
age. The waveform of the ERG changes from being a-wave dominated to
b-wave dominated, events that are paralleled by the development of the
outer plexiform layer.
Kittens are born
with an immature visual system that requires about 4 months for maturation.
Photoreceptors are mature by the end of the first month and the remainder
of the maturational process occurs in more proximal elements such as
ganglion cells. Development of the electroretinogram in kittens has
also been reported to occur in phases. The first stage is marked by
the b-wave appearance during the first 10 days after birth, and the
second phase corresponds to the increase in amplitude of the b-wave
(10-49 days). The b-wave evoked by high intensity stimulation matures
by 5-7 weeks of age whereas maturation of the b-wave evoked by low-level
stimulation requires an additional 3-5 weeks.114 The third phase is
required for attainment of adult implicit time values and oscillatory
potential development.114 A study of cone b-wave maturation in kittens
revealed that between 25 and 94 days of age, the amplitudes were either
normal or greater than normal.115 Adults values for the b-wave were
attained after 100 days, implicit times reached adult levels by 80 days,
and flicker fusion matured at about 74 days of age. As in dogs, maturation
in the cat includes ages at which the b-wave amplitudes are greater
than those expected in adults. Some have suggested that there may actually
be more functional cells in the retina than in adults during those periods
and that the decline to adult values is a reflection of normal degeneration.115
The manner in which
the canine retina responds to a flickering stimulus also changes with
maturation and permits an evaluation of rod and cone function.113 The
cone branch of the FFRC is present first at 16 days of age and by 30
days, the FFRC was clearly bipartite. The break point between rod and
cone branches occurred at lower intensity levels and by 60 days, the
values were essentially the same as adults. Oscillatory potentials appear
on the b-wave of the ERG at about 3 weeks of age with high light intensities.116
By 11 weeks of age, the potentials were well-developed and became apparent
with lower intensities.
of VEP in puppies was reported to begin as early as the second day after
birth with a negative wave characterized by a latency that exceeded
500 msec.98 By day 3 or 4, the peak had shortened and this was followed
by the addition of another negative peak. The number of peaks increased
between 2 and 3 weeks of age, which was accompanied by a decrease in
peak latencies. By the 5th week, the response simplified somewhat with
considerably shortened latencies. In a subsequent study conducted in
puppies from 7 to 100 days of age, it was shown that the latency for
P1 of the VEP was mature as early as 11 days and 38 days was required
for the latency of N1 and P2.117 The latencies of N2 and P3 were not
mature by the end of the study. During the first 5 weeks after birth,
the maturation of the VEP closely parallels neuronal development in
the visual cortex.95 Generally, VEPs in maturing animals are more variable
between individuals and more fatigable than in adults.97 Long latency
visual evoked responses appear in the feline visual cortex on or about
the second day of life and short latency responses at 5 days to 2 weeks
of age.118 The first potnetial reported to appear was a negative wave
that would become the N2 in the adult.119 The second potential was N1,
which occurred between 5-8 days of age, and then P1 preceeded N1 by
The long latency
response resembles that in an adult cat between 30-40 days. Between
14 and 20 days, kittens begin to visually locate or avoid objects.120
Postnatal development of OP in kittens follow the same general course
as ERG and VEP. Prior to 7 weeks of age, the OP differed from adults
in numbers, amplitude and time between peaks.114 By 18 weeks of age,
values were similar to those of adults. Sequential maturation of VEP
components was reported in lambs during the first 30 days after birth.111
The early component, N1, did not show a significant decrease in latency
whereas the later potential, P2, did. This was taken to mean that the
primary nerve tracts (N1) were mature at birth, but increasing myelination
and integration in the cortex accounted for shorter latencies for P2.
of the ERG in The Diagnosis of Retinal Diseases
Progressive Retinal Atrophy
Electroretinography has became an essential diagnostic aid for several
retinal diseases in veterinary species. Among those that have been documented
are rod-cone dysplasia, pigment epithelial dystrophy or central progressive
retinal atrophy, rod dysplasia, and hemeralopia. In most of these, except
pigment epithelial dystrophy, the photoreceptor layer is affected first
with secondary degeneration of remaining retinal layers. Progressive
retinal atrophy (PRA) refers to inherited diseases that are characterized
by degeneration or dysplasia of the retina. These abnormalities are
progressive and result in more or less predictable visual deficits much
like retinitis pigmentosa in human beings.29, 121 The different varieties
of PRA differ in onset and severity of ophthalmic, behavioral, and electroretinographic
changes, and the layers of the retina that are involved.
atrophy has been classified as generalized PRA (GPRA) in which the photoreceptors
are affected and central PRA (CPRA), in which the neural retina degenerates
secondary to the pigment epithelial layer. Generally, the early ophthalmoscopic
signs of GPRA include an increase in pupil size, increased reflectivity
of the tapetal fundus, retinal vascular attenuation. Nyctalopia is usually
the first behavioral sign and vision may progress towards total loss.
As the visual defect progresses, the pupillary light reflex is depressed
with no accompanying anisocoria. Many types of PRA are inherited as
simple autosomal recessive traits.37 The specific characteristics of
PRA vary between breeds, and even within breeds different types have
been reported. In contrast to GPRA, CPRA is characterized by hypertrophy
of pigment epithelial cells.122 What begins as irregular pigment foci
in the tapetal region just above the optic nerve near the area centralis
progresses to include the entire pigment epithelium. Central PRA is
actually a type of retinal pigment epithelial dystrophy.
of PRA is based on age of onset and progression of the disease.113 The
photoreceptor dysplasias are those with an early onset and rapid progression.
The second group consists of those diseases characterized by abnormal
photoreceptor development which occurs early but progress slowly. Those
retinal degenerations with a late onset and slow progression constitute
the third group. Clinical onset can be as early as 6 weeks in the Norwegian
Elkhound.113 6-8 weeks in the Irish Setter123, 6 months in the longhair
Dachshund124, ten months in the Tibetan Terrier37, 2-3 years in Samoyeds,
and 3-5 years in Miniature Poodles.125
signs of disease are often undetectable in puppies affected with PRA,
the ERG is the only method of early diagnosis. In fact, the majority
of the reports in the veterinary literature that pertain to the clinical
use of the ERG deal with some form of PRA. The age at which PRA is electroretinographically
confirmed varies with the type of PRA and the breed in which it occurs
(Table I). In the Dachshund, the early development of the ERG is normal,
but changes appeared as early as 17 weeks. By nine months of age, ERG
were characterized by reduced amplitudes and prolonged latencies, or
extinguished altogether. Histopathologic changes, which precede clinical
or electrodiagnostic changes, appear as early as 9 weeks of age in Tibetan
procedures have been developed to take advantage of the way that PRA
affects certain species and breeds of animals. PRA may initially involve
both rods and cones, but in many cases, the progression in rods is greater
than in cones.37 An electroretinographic technique was proposed for
use in diagnosing rod dysplasia (RD) in 6-week-old Norwegian Elkhound
pups.141 After light adapting for 5 minutes against a background intensity
of 10 ft.-lamberts, the background was discontinued and red flashes
presented at 0, 1,2,3,10,15, and 20 minutes of dark adaptation. Last,
a white flash was presented after 20 minutes of adaptation. In normal
pups the initial photophic ERG was followed by the gradual development
of the scotopic ERG after 1 minute. As dark adaptation progressed, the
scotopic b-wave overwhelmed the photopic b-wave. In the RD-affected
puppies, the scotpic b-wave was absent and the photopic b-wave did not
change in form or amplitude during dark adaptation.
responses to flickering stimuli has also been used to diagnose early
retinal degeneration (ERD) in Norwegian Elkhounds.113 In affected dogs,
the responses were low in amplitude and failed to follow the stimulus
in a 1:1 manner. The responses were initially corneal-positive (b-wave
dominated), but gradually became more corneal negative (a-wave dominated)
as maturation proceeded. In ERD-affected animals, the overall sensitivity
was reduced (curve shifted to the right), the rod branch of the curve
was lost, and the cone branch eventually failed (Fig. 13).113
was also useful in diagnosing progressive rod-cone degeneration (PRCD)
in miniature poodles.127 From 4-8 months of age, affected animals had
normal ERGs, but a reduction in rod responses were obvious between 12-16
months while cone responses were normal. Eventually cone responses showed
abnormalities even though implicit times remained normal.
In miniature poodles
and English cockers, the ERG is characterized by a loss of rod function
with preservation of cone function. The changes, which consisted of
reduced amplitudes and prolonged implicit times, were obvious in dogs
ranging in age from 9-28 weeks. In Tibetan terriers, ERG changes were
not apparent until approximately 10 months and consisted of changes
in the amplitude only.37 The same pattern is seen in American and English
cocker spaniels in which the onset may be seen between 2-3 years. The
onset in American cockers may be slightly earlier than in English cockers.142
cats have also been reported which, like dogs, are characterized by
loss of rods and cones and by thinning of the outer nuclear layer of
the retina.15 The fundus appeared devoid of blood vessels but without
optic atrophy. The cause of some concern was the coincident absence
of a recordable ERG but the presence of a pupillary light reflex using
bright light. Retinal degeneration has also been reported in Abyssinian
cats in which the electrophysiologic characteristics of the disease
were similar to retinitis pigmentosa in human beings.14 There was no
change in the waveform or implicit times in affected cats, but the amplitudes
of the a- and b-waves were diminished. In kittens that were 8-16 weeks
of age, there was a decrease in the maximum dark adapted (45 minutes)
b-wave amplitude, but not the a-wave. This occurs at a time when retinal
sensitivity is also slightly decreased.
has also been performed in Rdy cats which are affected with rod-cone
dysplasia (Rdy is the gene symbol).116 In 4.5 week-old kittens, the
ERG was absent or just barely recordable using contact lens electrodes,
but were recordable using intravitreal needle electrodes. Using this
technique, the ERG was devoid of oscillatory potentials, the a-wave
dominated the ERG, both a- and b-waves had reduced amplitudes and prolonged
implicit times, the b-wave threshold was higher than the a-wave threshold,
and photopic ERG could not be recorded. The a-wave domination seemed
to point to defective synaptogenesis in the outer plexiform layer or
dystropic retinas. Even using the intravitreal technique, ERG could
not be recorded at 7 months of age. In displaying an a-wave dominated
ERG, the Rdy cats were like Norwegian Elkhounds affected with early
retinal degeneration, but unlike them in having prolonged implicit times.
Hemeralopia is a retinal disease characterized by the progressive loss
of cone photoreceptors. The behavioral sign is obviously day-blindness
or inability to see in areas where there is a high level of artificial
light. The electroretinogram reveals the absence of cone function while
rods continue to function normally. Scotopic flicker fusion was used
to identify hemeralopia in Alaskan Malamutes as early as 6 weeks of
age.12 Hemeralopia was confirmed if flicker ERGs were not recordable
at 20 flashes/sec (fps). In Malamutes that were behaviorally day-blind,
flicker responses were not obtainable at a frequency above 10 flashes
per second.126 Non-hemeralopic dogs could still respond at frequencies
as high as 75 fps. There were no differences between affected and non-affected
dogs when using single flashes in dark adapted dogs. In 8-week-old Malamute
pups, flicker fusion frequency (FFF) was 5-15 fps and in the non-hemeralopes,
the fusion was between 44 and 75 fps.127 By 24 weeks of age, FFF was
76 fps in non-hemeralopes and 10-18 in the hemeralopes. In some pups,
FFF was high at 8 weeks of age, but fell to much lower rates by 24 weeks,
thus revealing its progressive nature.
Glaucoma and Sudden Blindness
Cataracts are often associated clinically with retinal degeneration
or retinal detachment. ERGs are usually recommended prior to cataract
removal because an opaque lens often prevents visualization of the fundus.
The only benefit in removing a cloudy lens from an animal with advanced
retinal dysfunction would be cosmetic. Cataracts are common in miniature
and toy poodles and mature quite rapidly. This rapid maturation prevents
an ophthalmoscopic confirmation of PRA. Cataracts alone will not necessarily
eliminate or even depress the ERG.12 In some cases, the presence of
a cataract will actually enhance the amplitude of the a- and b-waves.
The cataractous lens will scatter light more than a clear lens and the
end result is that more of the peripheral retina is stimulated.. A depressed
ERG in an animal with cataracts is usually a sign that there is some
form of retinal disease present. Because as many as 13.4% of the dogs
with cataracts also have some form of retinopathy, pre-surgical electroretinographic
evaluation of the retina is advised. Glaucoma has been shown to reduce
the amplitude of the b-wave and cause a prolongation of the a-wave,12
especially during the end stages of the disease when retinal damage
is the result of chronically high pressures. In Basset Hounds, Beagles,
and American Cocker Spaniel, glaucoma causes a depression in the a-
and b-waves of the ERG, which is detectable in pups that are 6-18 months
of age.7 Most of the reported diseases that cause blindness in dogs
have a gradual onset and in many breeds follow a predictable pattern
that includes electroretinographic changes. There is one form of blindness,
however, that has a sudden onset and does not appear to be breed-specific.
This acute form of blindness, which is called sudden acquired retinal
degeneration (SARD), is accompanied by an ophthalmoscopically normal
fundus and abnormal pupillary light reflexes.13 Electrodiagnostically,
this disease is characterized by bilaterally extinguished ERGs. Histopathologic
examinations of retinae from affected dogs reveal that retinal changes
are restricted to the photoreceptor layer whereas the inner layers of
the retinas are normal.143 There is some suspicion that the disease
has an autoimmune component in which affected dogs become sensitized
by their own retinal antigens.
Nerve Hypoplasia and Retinal Detachment
Optic nerve hypoplasia is not uncommon in dogs. This condition may be
inherited and does not always occur bilaterally. In dogs with hypoplastic
optic nerves, the principle histopathologic finding is a reduction in
the diameter of the optic nerves, chiasma, and optic tracts.6 The retina
is characterized by a reduced number of ganglion cells and decreased
thickness of the optic-fiber layer, but other layers appeared to be
normal. The ERG may be normal because ganglion cells and optic nerve
fibers do not directly contribute to the response.109 In some cases
however, ERGs were reported to have inconsistent a-waves, and there
was a progressive reduction in the a- and b-waves and the flicker-fusion
was low. These findings were taken as evidence of additional retinal
disease that was not described by light microscopy.6 The ERG can be
combined with ultrasonography to detect retinal detachments. In most
cases, the ERG waveforms are diminished early, but disappear altogether
in the later stages.7 In some cases, the ERG may be recordable in cases
of retinal detachment, but the b wave may be absent leaving only the
E Deficiency Retinopathy
Puppies fed a vitamin E deficient diet have been reported to show ophthalmoscopic
signs of retinopathy beginning as early as 3 months after weaning.144
Early signs began around the central artery with mottling or stippling
in the deeper layers of the retina. After dogs had been vitamin E deficient
for 4 months, the mottling worsened and ERGs were not recordable. Dogs
were clinically blind in dim light, but not in bright light. Vitamin
E supplementation for the next 2 months resulted in the return of ERGs
with diminished a- and b-wave amplitudes. Prolonged vitamin E deficiency
did result in permanently extinguished ERGs.
Equine night blindness (ENB) has been reported to occur in Appaloosas
with an onset as early as one month of age.145 The ERG in a foal that
showed obvious night blindness was reported to consist of a long, slow
negative wave that consumed approximately 400 msec. This pattern has
been called a "negative ERG," and taken as a physiologic indicator of
scotopic function. The proposed cause of ENB is a neural transmission
defect in the region of the inner segments of the photoreceptors or
in the region of the bipolar cells.
Degeneration in Cattle
Blindness in Hostein-Friesian cattle was reported to be related to diffuse
hydropic degeneration of ganglion cells accompanied by the invasion
of melanin in the nerve fiber layer, loss of photoreceptors, and thinning
of nuclear layers.64 Affected calves also showed evidence of internal
hydrocephalus and cerebellar hypoplasia at necropsy. In the same study,
blindness in Japanese Black cattle was apparently related to thinning
of retinal nuclear layers, vacuolar degeneration of Muller cells and
absence of photoreceptors. The ERGs and OPs in blind calves were either
non-recordable or had reduced amplitudes.
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Surg., 1:226, 1977. Figure Legends
Figure 1. The components of a typical vertebrate electroretinogram.
Figure 2. ERG recorded from a normal adult dog that was dark-adapted
for 5 minutes. The light stimulus was a white stroboscopic flash. Vertical
divisions = 48.8 IV; horizontal divisions = 60 msec.
Figure 3. ERG recorded from a normal adult dog that was light adapted.
Vertical divisions = 48.8 IV; horizontal divisions = 60 msec.
Figure 4. Relationships of frequency for flicker fusion with log luminance
of light flashes. The graph represents on the ordinate: The maximum
frequencies of light flashes which caused a flicker response for particular
luminance of the flashes plotted in log10 units on the abscissa. Each
point of the curve represents mean values and standard deviation of
7 dogs. Note the slowly rising slope for dim light flashes indicative
of rod function and the steep slope for bright stimuli indicative of
additional cone function. (From Liverani, F. and Schaeppi, U.: Pharmac.
Ther. 5:599, 1979.)
Figure 5. ERG waveforms recorded by scotopically balanced blue (right
column) and red (left column) stimuli. Top row was recorded in the dark
adapted state. Responses recorded in the presence of increasing intensity
of blue-green background light (Wratten No. 45) are shown successively
in the 2nd to 7th traces. The numbers on the left indicate the log relative
intensity of the background light. The bottom trace shows the time course
of the stimulus. (From Yanase, J., et al.: J. Vet. Med. Sci. 57:877,
Figure 6. Canine electroretinogram (ERG) intensity series recorded in
the dark-adapted state with 8-millisecond (msec) white stimuli. The
numbers on the left indicate the logarithm of the relative stimulus
intensity. The bottom trace shows the time course of the stimulus. STR
= scotopic threshold response. (From Yanase, J., et al.: Am. J. Vet.
Res. 57:361, 1996.)
Figure 7. PERG recorded from one dog as a result of visual stimulation
with vertical grating patterns at spatial frequencies ranging from 0.015
(bottom) to 0.96 (top) cycles per degree of visual angle. Each trace
is an average of activity resulting from 512 separate stimuli. Overlaid
traces at each frequency are replicates. Peaks N1, and N2 are labeled.
Horizontal division = 50 msec; vertical division = 0.61mV. (From Sims,
M.H. and Ward, D.A.: Prog. Vet. Comp. Ophthalmol. 3:106, 1993.)
Figure 8. Oscillatory potentials (OP) recorded from a cat (top) and
a dog (bottom) in response to a single white stroboscopic flash after
dark adaptation. Frequency bandpass = 100-500 Hz. Positive peaks are
labeled O1 through O4 and O5 for the cat and dog, respectively. Arrow
= flash discharge; horizontal division = 25 msec; vertical division
= 12.2mV (top) and 9.76mV (bottom). Figure 9. Electroretinogram (top)
and oscillatory potentials (bottom) recorded from a cat after 60 minutes
of dark adaptation. Recordings are averages of four responses, elicited
by stroboscopic flashes presented at 30-second intervals. ERG a- and
b-waves are labeled; individual OP peaks are labeled O1 through O4.
Vertical division = 122.06mV (top) and 12.2mV (bottom). Horizontal division
= 25 msec. Arrow = flash discharge. (From Sims, M.H., et al.: Prog.
Vet. Comp. Ophthalmol. 3:177, 1991.)
Figure 10. Visual evoked potentials recorded from electrode pairs O1-Ch
in 3 dogs as a result of stimulation of the right eye with a 3x5 matrix
of light-emitting diodes. Electrode O1 was 2-3 cm to the right of the
midline and about 2/3 of the distance from a point between the eyes
and the occipital protuberance; electrode Ch was on the midline in the
lower jaw. Each trace is an average of 256 recordings. Horizontal division
= 25ms; vertical division = 0.6mV. (From Sims, M.H., et al.: Am. J.
Vet. Res. 50:1823, 1989.)
Figure 11. Electroretinograms (ERG) and visual-evoked potentials (VEP)
resulting from monocular stimulation of the left eye. Electrode pairing
is shown. Two VEP are overlaid for each electrode pair; each trace is
an average of 128 recordings. Abiscissa = 40 ms/division, ordinate =
6.1mV/division for electrode pairs Cl-Al and Cl-Ch and 1.5mV for all
remaining pairs. (From Sims, M.H. and Laratta, L.J.: Am. J. Vet. Res.
48:1876, 1989.) Figure 12. Potentials recorded from electrode pairs
Fpz-Ch, Fz-Ch, Cz-Ch, and Oz-Ch in 3 dogs. Fpz was located midway between
the eyes, Oz was located over the occipital protuberance, Fz was one-third
of the distance between Fpz and Oz, Cz was two-thirds of the distance
between Fpz and Oz, and Ch was on the midline in the lower jaw. Each
trace is an average of 256 recordings. The recording at Fpz was an ERG
and the recordings at Cz and Oz were clearly VEP. The recording at Fz
sometimes resembled an ERG and sometimes resembled a VEP. Horizontal
division = 25ms; vertical division = 0.6mV. (From Sims, M.H., et al.:
Am. J. Vet. Res. 50:1823, 1989.
Figure 13. Changes in the flicker fusion response curve with retinal
development in control (A) and erd-affected dogs (B). (A), in young
normal dogs, flicker responses are only elicitable with high-intensity
stimuli and the curve contains only the cone branch. By 30 days the
curve is bipartite; with time, peak fusion frequencies increase at each
intensity level and the rod-cone break point shifts to the left. (B),
erd-affected dogs have a bipartite curve, but the rod-cone break point
is displaced to the right on the intensity axis. The rod branch never
matures and is lost by 89 days. The cone branch degenerates slowly and
responses are only recordable in the older affected animals (103-285
days) using maximal light intensities. For comparison, previously published
(Aguirre, 1978) flicker data for rod dysplasia (rd) affected Norwegian
elkhounds are included. In this disease, the rod branch is non-recordable
while the cone branch is normal. (From Acland, G.M. and Aguirre, G.D.,
Exp. Eye. Res. 44:491, 1997.
Table I. Breeds
Affected by Retinal Diseases and Ages at Which Behavioral, Ophthalmoscopic
and Electroretinographic Signs Appear Breed Type of Retinal Disease
Age at Which Behavioral Visual Deficits Appear Age at Which OphthalmoscopicSigns
Appear Age at Which Electroretinographic Procedures Provide Diagnostic
Information Photoreceptor Dysplasias Alaskan Malamute3, 126, 127 Progressive
cone degeneration (Hemeralopia) 8-29 weeks 8-29 weeks 8-29 weeks. Responses
that elicit rod ERG were normal; cone branch of the flicker fusion response
was absent; dark-adapted response to white light normal; responses to
flicker extinguished at rates greater than 25 fps. Belgian Shepherd128
Photoreceptor dysplasia 8 weeks 11 weeks 4 weeks. ERG extinguished.
Collie129 Rod-cone dysplasia (type 2) 6 weeks 3-4 months 16 days. Deficient
ERGs in light and dark adapted pups; rod ERG failed to develop; cone
responses were abnormal and then degenerated. Greyhound130 Retinal Dystrophy
18-36 months 18-36 months 22 months. No photopic ERG; dark adaptation
did not increase ERG amplitude; flicker fusion rates were not recordable
due to low ERG amplitude. Irish Setter4, 123 Rod-cone dysplasia (type
1) 6-8 weeks 3-4 months 3-4 weeks. Absent rod responses; reduced cone
responses; abnormal flicker; increase in cone response implicit times
and decrease in amplitudes; reduced flicker fusion frequency and extinguished
by 18 weeks. Irish Setter (Red)131 Progressive Retinal Atrophy 6-8 weeks
6-8 weeks Not reported. Miniature Schnauzer132 Photoreceptor dysplasia
6-12 months 1-2 years 8 weeks. Rod and cone contributions to ERG reduced
early postnatally; responses abolished by 4-6 months of age; ERG amplitudes
low; waveform altered; low intensity red stimulus failed to elicit a
response at any stage of dark adaptation; most rod-flicker responses
were not recordable; cone-flicker present early but amplitude decreased
with age. Norwegian Elkhound113, 133 Early Retinal Degeneration 6 weeks
6 months 12 weeks. Failure of rod b-wave to develop; ERG was a-wave
dominant; scotopic blue response was absent; scotopic red and white
stimuli elicit low amplitude, short latency responses; absent rod branch
with flicker fusion; cone ERG eventually deteriorated; ERG extinguished
by 1 year of age. Norwegian Elkhound29, 31 Rod dysplasia 6 weeks 5 months
6 weeks. Absence of scotopic b wave during dark adaptation; abnormal
response to low-intensity flicker at a low frequency; decreased photopic
b-wave in adults, extinguished by 3 years of age. Breed Type of Retinal
Disease Age at Which Behavioral Visual Deficits Appear Age at Which
OphthalmoscopicSigns Appear Age at Which Electroretinographic Procedures
Provide Diagnostic Information Norwegian Elkhound31 Rod dysplasia 6
months 6 months 6 weeks. No response to low-intensity light in dark-adapted
dogs; diminished response to high intensity stimuli. Norwegian Elkhounds113
Early Retinal Degeneration 6 weeks 6 weeks?; 13.5 months 30 days. ERGs
low in amplitude; dark-adapted white-light responses were a-wave dominant;
b-wave amplitude never greater than a-wave amplitude; rod branch of
FFRC lost early, cone branch failed more slowly. Norwegian Elkhound134
Rod dysplasia 51 days. Rrod responses not recordable; rod branch of
flicker fusion response curve absent; elevated dark adapted threshold
Later-Onset Photoreceptor Degenerations Akita128, 135 Progressive retinal
atrophy 2-3 years 2-3 years 10 months. English Cocker Spaniel128 Progressive
rod cone degeneration 3-5 years 3-5 years 12 months. Labrador Retriever46
Generalized Progressive retinal atrophy 3-5 years 3-5 years 3 years.
Reduced a- and b-wave amplitudes; a- and b-wave latencies unaltered;
photopic flicker normal early but later isoelectric at 30 fps. Miniature
Longhaired Dachshund124 Progressive retinal atophy 6-9 months 6 months
17 weeks-9 months. Decreased amplitudes; increased implicit times; no
evidence of rod loss; ERG extinguished in some cases. Miniature Poodles125,
136 Progressive rod-cone degeneration 28 weeks-12 months. Reduction
in scotopic b-wave amplitudes; severely depressed by 18 months; full
field ERGs had reduced rod amplitudes; normal cone amplitudes; progressed
to include cones; implicit times always normal. Miniature Poodles53
Progressive Retinal Atrophy 9 ½ weeks. Increase in b-wave implicit times
and decreased b-wave amplitudes; increased flicker thresholds. Samoyed137
Progressive retinal atrophy 2-4 years 2-3 years 16-24 months (decrease
in a and b waves, especially scotopic b wave. Breed Type of Retinal
Disease Age at Which Behavioral Visual Deficits Appear Age at Which
OphthalmoscopicSigns Appear Age at Which Electroretinographic Procedures
Provide Diagnostic Information Swiss Hound138 Progressive Retinal Atrophy
4 years 4 years 4 years. ERG not recordable even with light of strong
intensity; SP recording was flat Tibetan Terrier139 congenital stationary
night blindness (CSNB) Not Reported 10 months 10 months. a- and b-waves
recognizable; large negative after potential after the b-wave; some
ERG showed almost complete loss of b-wave; b-wave implicit times not
affected; loss of all positivity with light adaptation; low amplitude
responses with flicker. Tibetan Terrier37 Progressive retinal atrophy
1-2 years 12-18 months 10 months. Small changes early in the disease
but leading to reduction in the scotopic b-wave amplitude and then complete
dextinction; flicker amplitudes were reduced. Retinal Pigment Epithelial
Dystrophies Collie breeds128 Central progressive retinal atrophy 18
months onward Not informative. Briard128, 140 Congenital Stationary
Night Blindness (CSNB) 7-12 months 18 months onward 7-12 months. (Failure
of a- and b-waves during dark-adaptation or very small responses; affected
dogs responded to 3-Hz flicker, but amplitudes reduced 50-70%; Not informative
Labrador Retriever128 Central progressive retinal atrophy 18 months
onward Not informative