EFFECTS OF BILATERAL CALORIC HABITUATION ON NYSTAGMUS 

RESPONSES OF THE CAT 

MARY JAYNE CAPPS and WILLIAM E. COLLINS 

It has been suggested that the decline (habituation) of the nystagmus response to repeated vestibular stimulation is a form of learning in that it possesses the necessary features of 

a learned behavior-acquisition, retention, and 

transfer (Halstead, 1935). Acquisition of habituation is evidenced through the progressive 

reduction of the response with repeated stimulation, while retention has been reported for 

periods as long as several weeks (Halstead, 

1935; Henriksson, Kohut, & Fernandez, 1961). 

Transfer of unilateral caloric nystagmus habituation was shown to occur when a previously non-stimulated ear was irrigated with 

a stimulus provoking a response in the same 

direction as that elicited during habituation of 

the contralateral ear, responses elicited in the 

unhabituated direction were reported to be 

vigorous (Collins, 1964a; Henriksson, Kohut, & 

Fernandez, 1961). This apparent directional 

specificity of transfer has also been shown for 

(bilateral) habituation to mild angular acceleration (Crampton, 1962). However, studies 

have generally reported a failure to obtain 

' A major portion of the data presented here was submitted by the first-named author to the Psychology Department, University of Oklahoma, in partial fulfillment of the 

requirements for the degree of Master of Science. Grateful acknowledgement is made of the assistance rendered 

by Joseph E. Duchon, Billy P. Updegraff, Stanley Evans, 

and Mary Ellen Allen. 

transfer of habituation from one means of 

stimulation (e.g., rotatory) to another (e.g., 

caloric), in spite of the fact that both types of 

stimuli evoked responses in the same direction 

(Collins, 1964a, b; Hood & Pfaltz, 1954; Maxwell, Burke & Reston, 1922) The single study 

reporting a stimulus-transfer effect (from caloric to rbtatory stimulation) used extensive irrigations of ice water to abolish completely the 

nystagmus response (from each ear separately) 

before the rotation trials were administered 

(Dunlap, 1925). 

The present study was designed to examine 

some aspects of transfer of nystagmus habituation. Bilateral caloric irrigations (warm water 

in one ear, cool in the other) were employed 

to provide simultaneous deflection of the cupulae. Transfer of the response decline was 

checked by administering unilateral irrigations 

following different series of bilateral calorizations. Subsequent testing permitted an evaluation of various other aspects of vestibular 

habituation. 

ME mOD 

Sixty cats, unused in previous experimehts, 

served as subjects. The animals, restrained by 

the method of Henriksson, Fernandez, and 

Kohut ( 1961) and with their heads elevated to 

an optimal position, were divided into 6 equaf 

-1-
groups. Each group underwent caloric habituation to different stimulus conditions. 

Stimulation. Three water baths were used. 

One was filled with ice water at a temperature 

of 4° C ( ± 0.5° C), while the remaining 2 

were equipped with Bronwill constant temperature circulators which maintained water temperature at 26° C and soc C ( ± 0.01 o C) respectively (approximately 12° C above and 

below the cats' body temperature). Rubber 

tubing with attached irrigation nozzles provided the means for introducing the stimuli 

to the ears of the animals. The rate of flow 

(and, therefore, the total volume of water) was 

high (approximately 12 ccjsec) to permit a 

ready monitoring by touch of the return flow 

from the ear and assure delivery of the stimulus 

in total darkness. 

Recording and Scoring. Nystagmus recordings were obtained with an Offner Type T 

Electroencephalograph (time constant: 3 sec), 

located in an adjoining room. The corneoretinal 

potentials were detected by needle electrodes 

inserted at the outer canthi of the cats' eyes. 

Records were scored from the point of stimulus termination for number of beats, duration 

of nystagmus, and slow-phase displacement of 

the eyes. The number of nystagmic eye movements (beats) was simply counted for each 

trial. Response duration was measured from 

the termination of the irrigation to the last beat 

of the primary nystagmus. 

The amount of slow-phase eye-movement was 

obtained in millimeters by measuring the vertical displacement of each nystagmic beat from 

the peak to the base line. These values were 

summed for each trial and transformed into 

degrees by means of calibration constants obtained with an optokinetic stimulator. The 

latter consisted of a drum, 2 1/2 ft high and 

4 ft in diameter, driven by a DC motor. Altemate black and white vertical ftripes covered 

the interior of the drum. Eye-movements induced by a constant rotatory velocity ( 4 rpm) 

of the drum were recorded and scored for each 

animal to obtain a calibration value relating 

degrees of eye-movement (assuming perfect 

following) to millimeters of pen deflection. 

Procedure. The 6 habituation procedures are 

shown in Table 1. Each procedure comprised 

18 trials; a pretest, 15 habituation trials, a post-1 

test (identical to the pretest), and a post-2 

test of a different intensity. In each case, a 

nystagmus to the left was induced. The pre-, 

post-1 and post-2 tests were unilateral irrigations, applied in all cases to the right ear. All 

trials were administered on the same day, at 

20 min intervals. The irrigation and recording 

periods were always in total darkness, but 

animals were in full-room illumination for a 

period not less than 5 min before a trial began. 

Four groups (AI, All, BI, Bll) were habituated to a series of 15 simultaneous bilateral 

irrigations of soc C in the left ear and 26° C 

in the right ear. In order to obtain some information concerning the effects of time-ofirrigation on response magnitude, the duration 

of the bilateral habituating stimulus was different for each of these groups (BI: 15 sec; 

Bll: 20 sec; AI: 25 sec; All: 30 sec). 

The bilateral habituation stimuli for groups 

AI and All were used to produce responses of 

greater magnitude than the unilateral irrigation 

( 26° C for 30 sec) administered as a pre- and 

post-1 test. Groups BI and Bll received bilateral habituation stimuli which were selected 

to produce less vigorous responses than a preand post-1 test of ice water ( 4 c C for 15 sec). 

Two control groups ( AC and BC) were habituated to unilateral irrigations identical to the 

pre-and post-1 test stimulus of their respective 

groups (AC: 26° C for 30 sec; BC: 4° C for 

15 sec). These control animals provided a 

measure of the level of response after unilateral 

habituation. Therefore, comparison of the post1 test responses of one set of experimental (AI 

and All) and control ( AC) groups provided 

the basis for examining the question of transfer 

of habituation from a bilateral caloric series 

to a less intense unilateral stimulus. Likewise, 

comparlsons of post-1 test responses of BI and 

Bll with those of BC indicated the extent of 

transfer from a bilateral habituation series to a 

more intense unilateral stimulus. 

The post-2 test stimulus for the A groups 

was the same as the pre and post-1 test stimulus 

of the B groups. The B groups received post-2 

tests identical to the pre- and post-1 tests of the 

A groups. 

-2-
TABLE I 

Schedule of Test Stimuli for Each Group 

Test 

Pretest Habituation Post-1 Post-2 

Group ( 1 trial) ( 15 trials) ( 1 trial) ( 1 trial) 

AC Unilateral Unilateral Unilateral Unilateral 

26°C -30 sec 26°C- 30 sec 26°C -30 sec IW -15sec 

AI Unilateral Bilateral Unilateral Unilateral 

26°C- 30 sec 25 sec 26°C -30 sec IW -15sec 

All Unilateral Bilateral Unilateral Unilateral 

26°C -30 sec 30 sec 26°C- 30 sec IW -15sec 

BC Unilateral Unilateral Unilateral Unilateral 

IW -15sec IW -15sec IW -15sec 26°C- 30 sec 

BI Unilateral Bilateral Unilateral Unilateral 

IW -15sec IW -15sec IW -15sec 26°C -30 sec 

Unilateral Bilateral Unilateral Unilateral 

BII I W -15sec 20 sec IW -15sec 26°C-30 sec 

Note.-All unilateral trials were administered to the right ear. Bilateral trials consisted 

of simultaneous irrigations of 26°C (right ear) and 50°C (left ear). IW indicates ice water 

(4°C). 

RESULTS AND DISCUSSION 

I. Effects of bilateral caloric habituation on 

responses to unilateral stmulation. 

A GROUPS 

The experimental groups (AI and All) received habituation trials of greater intensity 

than the pretest and post-1 test. Figure 1, 

nystagmus tracings from an animal in group 

All, shows the variation in response magnitude 

to the bilateral and unilateral stimuli. 

Habituation Series. Figure 2 shows the declining mean response-per-trial of the A groups 

plotted as percentages of the pretest score. 

analyses of variance were conducted on those 

data for trials 1 and 15 (see Table 2). For the 

three A groups, the habituation series produced a statistically significant reduction in 

slow-phase displacement and number of beats 

( .001 level), but not in response duration. Previous studies have indicated that duration tends 

to be the least reliable measure of response decline (Fernandez & Schmidt, 1962; Henriksson, 

1956; Ward & Fernandez, 1963). 

Significant differences were also found among 

the groups for slow-phase displacement ( .05 

level) and number of beats ( .01 level). Multiple comparisons were made ( .05 level) with 

the Duncan test (Edwards, 1960). These comparisons showed that the control group yielded 

fewer beats and less slow-phase output than 

did either experimental group. Although the 

experimental groups did not differ significantly 

from each other in slow-phase displacement, 

group All tended toward greater slow-phase 

output, and produced a significantly greater 

number of nystagmic beats than did AI. These 

relations are evident in the curves of Figure 2 

in which there are 3 distinct levels of response 

in the number-of-beats graph, 2 in the slowphase graph, but no distinct differentiation of 

the groups in the duration data. 

-3-
TltiAL 

PRE 

5 

10 

15 

POST-I 

POST-2 

TEST SERIES: 26"C UNILATERAL 

HABITUATION SERIES• 30 SEC BILATERAL 

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TEST SERIES • ze•c UNILATERAL 

TEST SERIES: IW INLATERAL 

•L... 

CAT NO. AD-18 •• 

FIGURE 1. Recorded nystagmus from a cat in group All. Upward deflection of the pen denotes a movement of the eyes to the right; downward deflection to the left. 

Vertical bars through the tracings mark the termination of the stimulus. The 

bilateral habituating stimulus was more intense than that of the unilateral preand post-1 tests. 

-4-
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FxcVRE 2. Mean slow-phase eye-movement, number of beats, and response duration of the A 

groups plotted as percentages of the pretest score. Groups AI and All received 

bilateral habituating stimuli of greater intensity than the unilateral habituating 

stimulus applied to AC. 

-5-
TABLE 2 

Results of the Analyses of Variance on Percentage-of-Pretest Nystagmus 

Scores for Habituation Trials 1 and 15 of the A Groups 

Slow-Phase 

Source !!!__ MS F 

Groups (G) 2 27454.59 4.51° 

Subjects 

within G 27 6089.20 

Trials (T) 1 115246.92 34.12000 

TXG 2 3477.10 1.25 

T X Ss 

within G 27 91195.37 

All groups exhibited the greatest amount of 

decline in the first 5 trials of the habituation 

series (Fig. 2). Other studies have noted this 

characteristic of the response curves of habituation to unilateral caloric stimulation and 

to angular acceleration (Collins, 1964a, b; 

Griffith, 1920). 

Pretests and post-1 tests. The stimulus for 

the pre- and post-1 test for all A groups was a 

26° C unilateral irrigation for 30 sec. In order 

to determine the influence of the bilateral habituation trials on responses to the less intense 

unilateral stimulus, analyses of co-variance 

were conducted on the pre- and post-1 test 

scores for the slow-phase, number of beats, 

and duration measures (see Table 3). No 

significant differences were found among the 

three A groups on any measure. That is, habituation to bilateral caloric stimulation transferred to a unilateral irrigation of lesser 

intensity. 

Post-2 tests. The post-2 stimulus for the A 

groups was a 15 sec unilateral ice water ( IW) 

irrigation. For all groups, the response to the 

IW trial was greater than that to the post-1 

( 26° C) stimulus (see Fig. 2) . The increased 

amount of response to the IW trial was notably 

marked for the AC (control) group. 

Nystagmus Measure 

Frequency Duration 

MS F MS F 

15730.84 7.2900 1714.02 .78 

2158.45 2190.74 

51205.13 36.47° 00 11056.84 .86 

101.90 .73 547.29 .42 

1403.88 12902.60 

B GROUPS 

The experimental groups ( BI and BII) received pretests and post-1 tests of greater intensity than the habituation trials. Nystagmus 

tracings depicting this relation appear in 

Figure 3. 

Habituation series. Reduction of the nystagmic response occurred in each group as a result of the repeated trials of the habituation 

series. In Figure 4 the data are plotted as percentages of the pretest response and statistical 

analyses were conducted on these scores for 

trials 1 and 15 (see Table 4). Reductions in 

response significant at the .OOllevel were found 

for slow-phase displacement and number of 

beatS'. Duration data which were highly variable yielded no significant differences. The 

significant interaction effect ( .05 level) appears to be a result of differences in the slopes 

of the habituation curves (see Fig. 4). 

Differences significant at the .01 level were 

found among the B groups on all 3 nystagmus 

measures and multiple comparisons were made 

( .05 level) with Duncan's test (Edwards 1960). 

These comparisons showed that the control 

group produced a significantly greater number 

of nystagmic beats and more slow-phase out-

-6-
TABLE 3 

Results of the Analyses of Covariance on Pretest and Post-1 

Test Nystagmus Scores for the A Groups 

Slow-Phase 

Source ~ MS F 

Nystagmus Measure 

Frequency Duration 

MS F 

Treatments 2 118,270.6 .95 

MS 

560.8 

483.0 

F 

1.16 884.4 .87 

Error 26 125,130.3 

Total 28 

[F.9SC2.2Bl = 3.37] 

put than did either experimental group; the 

experimental groups did not differ from each 

other in nystagmus production. Duration 

scores were significantly different among all 

groups with BC greater than BI or BII, and 

BI greater than BII. These differences are 

evident in the curves of Figure 4 which show 

3 levels of duration scores and 2 levels (control and experimental) for the slow-phase data 

and the number of beats. 

1,018.9 

Pretests and post-1 tests. The stimulus for 

these tests ( 15 sec unilateral IW irrigation) 

was of greater intensity than the habituation 

stimuli for the experimental groups (Figs. 3 

and 4). Analyses of covariance were conducted 

on the 3 types of nystagmus scores (see Table 

5). No significant differences were found 

among the groups. Thus, habituation to bilateral caloric stimuli transferred to a more intense unilateral irrigation. 

TABLE 4 

Results of the Analyses of Variance on Percentage-of-Pretest Nystagmus 

Scores on Habituation Trials 1 and 15 of the B Groups 

Nystagmus Measure 

Slow-Phase Frequency Duration -· 

Source df MS F MS F MS F 

Groups (G) 2 11888.78 8.56° 0 10348.36 8.53° 0 7069.34 8.8300 

Subjects 

within G 27 i389.41 1212.54 801.02 

Trials (T) 1 13231.35 35.29#0° 8623.21 32.23"' 00 914.94 2.67 

TXG 2 1611.30 4.30° 839.89 3.14 236.74 .69 

TXSs 

within G 27 374.88 2675.20 342.07 

"'p < .05, oop < .01, ooop < .001. 

-7-
TRIAL TEST SERIES • IW UNILATERAL 

PRE 

HABITUATION SERIES' 15 SEC BILATERAL 

10 

TEST SERIES• IW UNILATERAL 

POST·I 

TEST SERIES' 26"C UNLATERAL 

POST-2 ---+------------------------------

CAT NO. 81·86 

FIGURE 3. Nystagmus tracings of an animal in group Bl. Markings are the same as in 

Figure l. The bilateral habituating stimulus was less intense than that of the 

pre- and post-! tests. 

-8-
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111411l'IIDIIR•M• 

TRIALS 

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FIGURE 4. Mean slow-phase eye-movement, number of beats, and response duration of the B 

groups plotted as percentages of the pretest score. Groups Bl and BII received 

bilateral habituating stimuli of less intensity than the unilateral habituating 

stimulus applied to BC. 

-9-
TABLE 5 

Results of the Analyses of Covariance on Pretest and Post-1 

Test Nystagmus Scores for the B Groups 

Slow-Phase 

Source df MS F 

Treatments 2 3,249.9 1.52 

Error 26 2,139.1 

Total 28 

[F9s<•·••> = 3.37] 

Post-2 tests. The post-2 test stimulus for the 

B groups was a 26° C unilateral irrigation for 

30 sec. This was the weakest of all group B 

stimuli, and it uniformly produced the least 

response given by these animals on any trial. 

GENERAL DISCUSSION OF A AND B 

GROUPS 

A habituation series of bilateral caloric irrigations has a pronounced effect upon the 

vestibular response to a unilateral irrigation, 

regardless of differences in intensity. Statistical analyses showed that nystagmus responses 

to unilateral trials after bilateral habituation 

were not significantly different from the response level of animals habituated to that same 

unilateral stimulus. This finding, indicating a 

transfer of habituation, differs from the studies 

using rotation as the bilateral habituation stimulas (Collins, 1964b; Hood & Pfaltz, 1954; Maxwell, et al., 1922). In the latter instances, 

habituation to rotation had no marked reductive effect on subsequent unilateral caloric irrigations. The fact that intensity differences 

existed between the rotatory habituation stimuli 

and the caloric transfer tests apparently does 

not account for the minimal amount or absence 

of transfer reported. 

In the present study, intensity appears to be 

negligible factor in bilateral-to-unilateral transfer or caloric habituation, but it may have 

exerted influence in the unilateral-to-unilateral 

Nystagmus Measure 

Frequency Duration 

MS F MS F 

11,904.8 2.00 594.2 .15 

5,954.7 3,870.5 

situation. The latter effect is shown in the 

vigorous responses of group AC (habituated to 

26° C unilateral irrigations) to the post-2 unilateral stimulus of ice water. Although probably affected to some extent by the previous 

habituation trials, these IW responses did not 

appear to be markedly reduced (Fig. 2). 

The present data seem to offer some hypotheses concerning the reported failure of 

(bilateral) rotational habituation to transfer to 

(unilateral) caloric stimulation. It is possible 

that calorization (a gross stimulus compared 

to angular acceleration) activates neural elements in addition to those related to the lateral 

semi-circular canal; that exact placement of 

the head in the optimal caloric and in the 

optimal rotational positions is extremely critical: m that change in the position of the head 

significantly alters the pattern of stimulation 

from otolithic and proprioceptive receptors. 

One or a combination of these factors might 

cause sufficient changes in the neural patterning so that the stimulus generalization necessary for transfer of habituation does not occur 

( cf. Guedry, 1964). 

Duration of an irrigation has been occasionally regarded as a subordinate consideration 

(especially to temperature effects) in caloric 

stimulation. However, pilot studies conducted 

prior to the present experiments indicated differences in response magnitude of cats to 15 vs 

25 sec and 20 vs 30 sec bilateral stimuli, favoring the longer stimulus durations. The present 

-10-
experiment allowed comparisons of nystagmus 

output to less diparate bilateral irrigations, viz. 

15 vs 20 sec and 25 vs 30 sec. The former pair 

differed only in duration, and those data were 

highly variable. The 30 sec stimulus produced 

significantly more nystagmic eye movements 

than did the 25 sec stimulus, and although there 

was no statistically significant difference in the 

slow-phase data, there was approximately 30 

per cent more slow-phase output in the first 

few 30-sec trials. These data indicate that the 

duration of irrigation may have some effect on 

nystagmus production even with a difference 

as small as 5 sec. It is possible that more pronounced effects of stimulus duration would be 

evident with lower rates of flow. 

II. Effects of bilateral caloric habituation on 

subsequent tests. 

DIRECTIONAL SPECIFICITY 

Twenty min after receiving the treatments 

noted above, 2 groups, AC and BI, were given 

10 additional habituation trials (with the usual 

interstimulus intervals) provoking responses in 

the direction opposite to the original habituation series. This was accomplished by stimulating the left ear of cats in the (unilateral habituation) AC group with 26° C irrigations for 

30 sec, and by interchanging the temperatures 

(to 26° C left ear and 50° C right ear for 15 

sec) for cats in the (bilateral habituation) BI 

group. Figures 5 and 6 show the mean response curves of both groups for the original 

and the subsequent habituation series for the 

3 scored measures. The curves for number of 

beats and slow-phase eye movement exhibit a 

common characteristic, that is, the marked drop 

in response within the first 3-4 trials of the 

subsequent habituation series, in contrast with 

the more gradual decline of the original series. 

Responses to the first trial for each direction 

of nystagmus are of about the same magnitude 

for group AC, yet the response output drops 

more rapidly during the early trials in the subsequent tests. A similar effect was observed in 

the data obtained from group BI, although here 

the beginning levels of the 2 habituation series 

are somewhat different. Group BI received 

an IW pretest irrigation, and this intense stimulation probably reduced the response to the 

first habituation trial. In spite of the differences in the initial levels, the BI curves for 

the second set of habituation trials exhibit the 

same exceptionally rapid early decline as that 

noted for group AC. However, the response 

for both groups AC and BI do not continue to 

drop at this rapid rate but, rather, level off so 

that the response to trial 10 of the subsequent 

series is at the same output level as trial 10 of 

the original series. 

Previous studies (Collins, 1964a; Crampton, 

1962; Henriksson, Kohut, & Fernandez, 1961) 

have indicated the apparent independence of 

direction with regard to vestibular habituation, 

that is, habituation of nystagmus in one direction did not appear to effect the response in 

the non-stimulated direction. These reports 

were based on a single stimulation in the previously unhabituated direction. In the present 

study, although the first response in the previously unhabituated direction was quite vigorous, responses to the following 2 or 3 irrigations dropped very rapidly, quite unlike the 

original decline. Thus, it would seem that the 

first habituation sequence did affect the responses in the non-stimulated direction. This 

apparent bi-directional effect of uni-directional 

habituation may be an extension of the transfer characteristic of the learning process postulated earlier (Halstead, 1935), in that the 

animal has learned to control the response to 

a method of stimulation. The absence of transfer effects on the first trial in the previously 

non-stimulated direction may be partly a result of the novelty of the first irrigation which 

deters the appearance of learning on that trial, 

but the effects become more apparent in succeeding trials. 

It should be noted that, after the original and 

subsequent habituation trials, an additional 

trial, identical to those of the original habituation series was performed for each animal. 

Responses were still at the habituated level. 

This retention by the cat of habituation in one 

direction, despite subsequent habituation in 

the other direction, confirms the report of 

Henriksson, Kohut, and Femandez ( 1961) but 

differs from findings reported for man ( Fluur & 

Mendel, 1962a, b). 

-11-
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GROUP AC 

80 STIMULUS • 21•c UMLATERAL 

"'- RIGHT EAR ::::>- ............ LEFT EAR :::E..J 70 <:> .. 

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I 2 3 4 5 6 7 8 9 10 II 12 13 114 t5 16 17 I 2 3 4 5 I 7 I I ~ 

T R A L S 

FIGURE 5. Trial-by-trial plots of nystagmus scores of group AC, in which habituation was 

produced for first one direction of nystagmus, and then the other. 17 unilateral 

irrigations of the right ear with a 26o C stimulus (and an 18th irrigation with 

IW not plotted) were followed by 10 left-ear stimulations. Note the high output 

on the first left-ear trial and then the rapid q'rop with succeeding trials. 

-12-
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GROU' 81 

~ SECOND 81LATERAL 

o------o R-26•c, L-to•c 

...___... R·tiO·c. L-n•c 

TRIALS 

r 1 s 4 51 1' •, t! 10 

FrcuRE 6. Trial-by-trial plots of nystagmus scores for group BI, in which habituation was 

produced for first one direction of nystagmus and then the other .. A function 

similar to that depicted in Figure 5 for group AC is evident for BI, although 

here the "first" trial is probably underestimated since it was preceded by an IW 

irrigation (arrow). 

-13-
RETENTION OF HABITUATION 

Rentention of nystagmus habituation has 

been reported for periods up to several weeks 

(Halstead, 1935; Henriksson, Kohut, & Fernandez, 1961). This temporal characteristic 

of habituation was investigated in group BC 

(habituated to 15 sec IW irrigations). Four 

animals from this group were tested one week 

afer, and 4 other cats 2 weeks after the original 

habituation series (see Fig. 7) . Retention was 

tested by 8 IW irrigations, in which the ear 

stimulated from alternated from trial-to-trial. 

Half of the animals began with a left-ear stimulation, the other half with a right-ear stimulation. Figure 8 shows the average responses on 

the initial series and on the retention series for 

the 3 scored measures. The small number of 

animals in each group prevented any reliable 

analysis of differences between the 1- and 2-

week periods and, since data obtained in the 

retention series were similar for both groups, 

they were averaged to provide a single response 

curve. Retention of habituation is apparent 

in the depicted differences for the habituated 

and unhabituated directions. 

The course of the response decline obtained 

in this retention series for the unhabituated direction is very similar to that representing the 

previously unhabituated responses of groups 

AC and BI in which the question of directional 

specificity was examined ( compare Figs. 5, 6 

and 7). Thus, responses of group BC to the 

several trials in the unhabituated direction 

provided additional evidence for some bidirectional effect of unidirectional habituation. 

HEAD POSITION 

The direction of the nystagmic response to a 

caloric stimulus can be reversed by a change 

in head position sufficient to alter the direction 

of endolymph flow. Twenty min after exposure 

to the habituation sequence previously described, the heads of animals in groups AI and 

BII were lowered so that the plane of the 

TRIAL STIMULUS: R- I W FOR 15 SEC 

17 

POST-I 

TWO WEEKS LATER 

STIMULUS : L-IW FOR 15 SEC 

STIMULUS: R-IW FOR 15 SEC 

CAT NO. BC-73 

... L_ 

.... 

FIGURE 7. Nystagmograms from a cat which received 17 unilateral IW irrigations. When 

tested 2 weeks later, the response in the habituated direction shows some recovery, but is clearly weaker than that of the unhabituated direction. Markings 

the same as in Figure 1. 

-14-
!!= 

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eo: lZ ... 

I!; I!; 

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"'"" "'"' 5~ 

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..,_ .. 

ID-

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:iii: 

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~I!; z,_ 

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l:l~ :s-

:::> 

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!!= 

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.... 

,,_ 

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..,o 

.,,_ 

h ,u 

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110 

100 

.. 

., 

70 

00 

70 

60 

!50 

40 

~I I 

130 

120 

110, 

.. 

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I 2 3 4 5 6 7 I 9 ~ II 12 B ~ e • 17 

• • 4 •• 1 • 9 K> II 12 13 14 .. .. 17 

""' 

GROUP BC 

STIMULUS • IW UNILATERAL 

HABITUATICIII TRtALS (RIGHT E.M) 

...__. RETENTION TRIALS (RIGHT EAR} 

......_,. RETENTION TRIALS {L£fT EAR) 

••••e•T•.• 

TRIALS 

\ ~ 

I •• 4 

~ \ 

I 2 • 4 v. I 2 •• 

I a I 4 

FIGURE 8. Retention of habituation in group BC. After initial unidirectional habituation 

(open circles), 4 cats were tested 1 week later and 4 others 2 weeks later 

(filled symbols) with nystagmus provoked in both directions. Data for the land 2-week groups were similar and are averaged here. The habituated response 

shows some recovery in the subsequent testing, but declines more rapidly than 

it did in the original series. The unhabituated direction yields more vigorous 

responses. 

-15-
horizontal canal was changed approximately 

180° from the previous test position; and 6 trials 

were administered. The first 3 "head lowered" 

irrigations for half of the animals in each group 

were identical to the original habituation stimulus (right ear-26° C, left ear-50° C), while 

the temperatures were interchanged for the 

last 3 trials. The order of presentation of the 

2 temperature-.combinations was reversed for 

the remaining animals. The lowering of the 

head changed the direction of nystagmus previously elicited by these stimuli. That is, with 

the head upright, cool water in the right ear 

and warm water in the left produced nystagmus 

to the left but with the head lowered, the 

same stimulus produced nystagmus to the right. 

Some animals did not respond to either 

stimulus when the head was tilted downward 

(perhaps, although it did not appear to be the 

case, due to inexact positioning). However, of 

the cats which did react, there was a definite 

directional difference as shown in Figure 9. 

These animals had been habituated to a stimulus provoking nystagmus to the left; when 

the same stimulus was administered with the 

head lowered, a vigorous response to the right 

was obtained. When the temperatures were 

interchanged, a reduced response in the habituated direction was elicited. The latter 

phenomena were also observed by Proctor and 

Fernandez ( 1963) who noted, in support of the 

notion that habituation is of central origin, that 

". . . the mechanism underlying habituation is 

operating on the neural system which determines the direction of nystagmus" ( p. 507). 

However, the responses produced with the 

head down in this study differed in appearance 

from those of the upright position, that is, the 

number of beats was greater and the amplitude 

was lower (see Fig. 9) . 

Another characteristic observed among 

groups receiving stimulation in alternating directions following habituation, was the apparent 

influence of the order of stimulation of the 

magnitude of the response. That is, there appeared to be less difference in the subsequent 

tests between the responses of the habituated 

and unhabituated directions when the first irrigation produced nystagmus in the previously 

habituated direction. Perhaps the novelty associated with the change of the head position 

served to heighten the first response elicited, 

regardless of the direction. However, this difference was only relative; the previously unhabituated direction uniformly yielded more 

vigorous responses. 

DOUBLE IRRIGATIONS 

Following habituation to 30 sec bilateral irrigations, animals in group All each received 2 

double irrigations (simultaneous bilateral calorizations of 26° C for 30 sec) at the usual interstimulus intervals of 20 min. With such stimulation, the horizontal component of nystagmus 

is ordinarily abolished and a vertical nystagmus 

usually appears. Since the horizontal component of the response had been subjected to 

uni-directional habituation, the double irrigations were administered to determine whether 

the nystagmus so elicited would evince a horizontal component in the unhabituated direc-

( see Fig. 10). Animals variously gave random 

eye movements or weak (prolonged, low velocity) responses in one direction or the other 

(some of which may have included a vertical 

component). 

Following the double irrigations, both directions were tested with 30 sec bilateral calorizations of 26° C and 50° C (the temperatures 

were interchanged to produce both directions 

of nystagmus). The order of presentation of 

the 2 bilateral irrigations was alternated from 

animal-to-animal. Responses in the habituated 

direction remained at a reduced level while 

responses in the previously non-stimulated direction were vigorous. 

III. Additional observations. 

SEX DIFFERENCES 

Of the 60 animals tested, 38 were females 

and 22 were males. Each male was matched 

with a female randomly chosen from the same 

group and t tests were conducted on the pretest 

nystagmus data (see Table 6). Female animals 

were found to produce a significantly ( .05 

level) greater amount of response as measured 

by both slow-phase displacement and number 

of beats. Although this may represent a true 

sex difference in vestibular functioning, it is 

-16-
TRIAL STIMULUS: R- 26°C, L- 50° C FOR 20 SEC 

15 

HEAD LOWERED 

STIMULUS= R-26°C, L-50°C FOR 20 SEC 

POST -3 

POST- 6 

STIMULUS= R- 50°C, L- 26° c FOR 20 SEC 

CAT NO. BIT - 93 so•.__l --

2 SEC 

FIGURE 9. Recorded nystagmus from a cat exposed to a habituation series of simultaneous 

bilateral calorizations with its head elevated. Lowering of the head changes the 

direction of nystagmus although the same stimulus is applied. Responses in the 

"practiced" direction are clearly weaker than those in the previously untested 

direction. 

-17-
TRIAL STIMULUS= R- 26°C, L-50°C FOR 30 SEC 

15 

STIMULUS= R-26°C, L-26°C FOR 30 SEC 

POST- 3 

STIMULUS R-26°C, L-50°C FOR 30 SEC 

STIMULUSt R-50°C, L-26°C FOR 30 SEC 

POST- 6 wN\f\f\NV\NMJ\N\f\NJ\NW~·NV\M!Wf'J\JVNWVVVW\N\ 

MM/VV JW\1\JV 

CAT NO. All- 62 so· l .... __ 

2 SEC 

FiGURE 10. Nystagmus tracings from a cat in group All. Post-3 and post-4 tests were 

"double irrigations" (simultaneous bilateral calorization with identical water 

temperatures) which yielded a weak and inconsistent left-beating nystagmus. 

Post-5 was identical to the habituation series and the response remained at 

its previous low level. In post-6, temperatures were interchanged, nystagmus 

was elicited in the opposite direction, and a vigorous response appeared. 

-18-
TABLE 6 

Results of t test Comparisons of Pretest Nystagmus 

Measures for 22 Male and 22 Female Cats 

Measure 

Slow-phase 

Frequency 

Duration 

t Value 

2.03 

1.76 

1.22 

Significance level 

.05 

.05 

t.05(42) = 1.675 

quite possibly due only to sex-related nonvestibular factors (e.g. density or mass of bone 

and other tissue) and may thereby be limited 

to caloric stimulation. There was no statistically significant sex difference in comeoretinal potential as determined by comparison 

of the calibration constants 

OPTOKINETIC NYSTAGMUS 

Nystagmographic recordings of eye-movements elicited by both clockwise and counterclockwise rotation of the optokinetic drum were 

obtained before and after the vestibular trials 

for 49 animals. Calibration constants calculated for each of these exposures were compared statistically to examine possible effects 

of the habituation series on the optokinetic response (see Table 7). No statistically reliable 

differences occurred as a result of the intervening vestibular stimulation, nor were any directional differences in the optokinetic responses evident. Figure 11 shows optokinetk 

nystagmus recordings for both directions before 

and after vestibular habituation. The tracings 

show no differences in the form or quality of 

the responses from one condition to another. 

INVERSE RESPONSES 

Two types of inverse vestibular responses 

were observed: secondary nystagmus and inverted primary nystagmus. Secondary nystagmus ( a response following, and in the direction opposite to the primary response) has been 

reported as a result of both rotatory and uniTABLE 7 

Results of the Analyses of Variance on Optokinetic Calibration 

Constants for Clockwise and Counterclockwise Drum Rotation 

Before and After Vestibular Habituation 

Source 

Order (0) 

Subjects 

within 0 

Direction (D) 

DXO 

D X Subject 

within 0 

[F.ssc1,se> = 3·

95] 

df 

1 

96 

1 

1 

96 

-19-

MS 

12147 

6937 

2096 

2682 

2711 

F 

1.75 

.773 

.989 
OPTOKINETIC NYSTAGMUS 

DRUM CW DRUM CCW 

BEFORE 

AFTER 

swl...l __ _ CAT NO. AI- 56 5 SEC 

DRUM CW DRUM CCW 

BEFORE 

AFTER 

CAT NO. 8 IT - 79 5 SEC 

FIGURE 11. Optokinetic nystagmus obtained from 2 cats. Drum speed was 24° /sec. 

lateral caloric stimulation in the cat (Collins, 

1964a, b). In the present study, secondary reactions occurred frequently ( 322 trials) in the 

tracings of 51 cats. The magnitude of these 

reactions ranged from "strong" to "very weak", 

and some of the latter may have represented 

induced spontaneous responses similar to those 

reported for man by Fluur and Mendel 

(196lb). 

The more intense stimuli appeared to elicit 

secondary responses more frequently, although 

there was no strict rank-order relation observed 

between stimulus intensity and number of occurrences. Fewer secondary reactions occurred 

as the number of trials increased. This decline 

of secondary nystagmus has been reported in 

recent studies of the cat for both rotatory and 

unilateral caloric stimulation (Collins, 1946a, b), 

but is not reported to occur in man ( Fluur 

& Mendel, 1962a, b). 

Although secondary nystagmus was not observed on every trial (a period of approximately 5 min), animals frequently exhibited a 

response in the direction of the secondary reaction 10-15 min after a stimulation, during the 

recording of the response of another animal 

( animals were tested in pairs ) . These late 

reactions (some of which may have been induced spontaneous nystagmus) occurred without additional stimulation, after a 5 min period 

in illumination, and ranged from a "strong" response (Fig. 12) to only one beat every 5-7 

seconds. The response shown in Figure 12 is 

the most vigorous of all the observed reactions 

of this type and therefore represents the extreme example. 

Inverted primary nystagmus (a response in 

the opposite direction of the expected primary 

which appears prior to, or instead of, a response 

approriate to the stimulus, Collins, 1963; Groen 

& Jongkees, 1949) was observed occasionally. 

Five animals exhibited occasional clear, though 

weak, inverted primary responses, in which the 

inverted beats were in evidence for 10-30 sec 

after termination of the irrigation. It is possible that these unusual responses are related 

to the delayed reactions noted above and depicted in Figure 12. 

-20-
TRIAL HABITUATION SERIES: 30 SEC BILATERAL 

WlvVIMNV\MMl\JNIIANMJ 

\fi-~~NJNM!Nt~ 

v~fi/1MNN,~~M~~. 

~~v~fJVw\IWIMNvV\ 

N\f\IV'!V\(\N\j1(llilvvVv\jt1JVI/{ v\,NV\11/Vv\('\;~ 

~-

~"~ VVVVV\/'··\iVV\iVv'v'VV\J\NV\'\jV~vVVvv'V\1\ 

4 

/I.NI(VVVV\N'vJ\/v~Vv\jv\fVV\i 

lfi/V\AJVV\MJ\j\J\/\I\jVI/vVVV v\/vV\/VI/IJ\(vVvV'vVVI/\/1/ 1/'V'J\.;~ 

CAT NO. A U-64 

FIGURE 12. Examples of inverse nystagmus. The tracings for trial 1 show vigorous primary 

and secondary reactions. The arrow indicates the start of secondary nystagmus; 

the jagged vertical line denotes a change of paper speed from 2.5 to 1.25 em/ 

sec. The tracing for trial 4 shows a brisk but reduced primary nystagmus; no 

secondary response appeared. Dots indicate the passage of approximately 10 

min (including 5 min in illumination) after which, without benefit of any 

additional stimulus, a vigorous response in the direction of secondary nystagmus 

appeared. The latter was recorded in darkness while another animal was being 

tested (paper speed: 2.5 em/sec). 

SUMMARY 

Transfer of bilateral caloric nystagmus habituation to unilateral calorization was investigated in a group of 60 cats. Habituation to 

bilateral caloric irrigations markedly reduced 

responses to both less intense and more intense 

unilateral stimulation. 

Subsequently testing provided information 

concerning the effects of caloric habituation 

on: ( 1 ) directional specificity of response, 

( 2) retention of the response decline, and 

( 3) optokinetic nystagmus. Statistical analyses 

also indicated a sex difference in response 

magnitude. 

REFERENCES 

Collins, W. E., 1963: Observations on the elicitation of 

secondary and inverted primary nystagmus from the 

cat by unilateral caloric irrigation. Aerospace Med., 34, 

1137-1142. 

Collins, W. E., 1964a: Nystagmus responses of the cat 

to rotation and to directionally equivalent and nonequivalent stimuli after unilateral caloric habituation. 

Acta Otolaryng. (in press). 

Collins, W. E., 1964b: Primary, secondary, and caloric 

nystagmus of the cat following habituation to rotation. 

]. comp. physiol. Psychol., 57, 417-421. 

Crampton, G. H., 1962: Directional imbalance of vestibular nystagmus in cat following repeated unidirectional 

angular acceleration. Acta Otolaryng., 55, 41-48. 

Dunlap, K., 1925: Adaptation of nystagmus to repeated 

caloric stimulation. ]. comp. Psychol., 5, 485-493. 

-21-
Edwards, A. L., 1960: Experimental design in Psychological research. New York: Holt, Rinehart, and Winston. 

Fernandez, C., and Schmidt, R., 1962: Studies on habituation of vestibular reflexes. II. Effect of caloric stimulation in decorticated cats. Ann. Oto-, Rhino-, Laryngol., 

71, 299-320. 

Fluur E. and Mendel, L., 1962a: Habituation, efference 

and vestibular interplay. I. Monaural caloric habituation. 

Acta Otolaryng., 55, 65-80. 

Fluur, E. and Mendel, L., 1962b: Habituation, efference 

and vestibular interplay. II. Combined caloric habituation. Acta Otolaryng., 55, 136-144. 

Griffith, C. R., 1920: The organic effects of repeated 

bodily rotation. ]. exp. Psychol., 3, 15-47. 

Groen, J. J. and Jongkees, L. B. W., 1949: The measure--

ment of the temperature at the eardrum during the 

caloric test of the labyrinth. ]. Physiol., 108, 33-36. 

Guedry, F. E., 1964: Psychophysiological studies of 

vestibular function: In W. D. Neff (Ed.). Advances 

in Sensory Physiology, New York: Academic Press. 

Halstead, W. C., 1935: The effects of cerebellar lesions 

upon the habituation of post-rotational nystagmus. Comp. 

Psychol. Monog., 12, 1-130. 

Henriksson, N. G., 1956: Speed of slow-component and 

duration in caloric nystagmus. Acta Otolaryng., Suppl. 

125, 20 pp. 

Henriksson, N. G., Fernandez, C., and Kohut, R. 1., 1961: 

The caloric test in the cat. Acta Otolaryng., 53, 21-32. 

Henriksson, N. G., Kohut, R. 1., and Fernandez, C., 1961: 

Studies on habituation of vestibular reflexes. I. Effect of 

repetitive caloric test. Acta Otolaryng., 53, 333-349. 

Hood, J. D., and Pfaltz, C. R., 1954: Observations upon 

the effects of repeated stimulation upon rotational and 

caloric nystagmus. ]. Physiol., 124, 130-144. 

Maxwell, S. S., Burke, U. L., and Reston, C., 1922: The 

effect of rotation on the duration of after-nystagmus in 

the rabbit. Amer. ]. Physiol., 58, 432-438. 

Proctor, L. R., and Fernandez, C., 1963: Studies on 

habituation of vestibular reflexes. IV. Effect of caloric 

stimulation in blindfolded cats. Acta Otolaryng., 56, 

500-508. 

Ward, P. H., and Fernandez, C., 

studies on vestibular mechanisms. 

ponderance of nystagmus in cats. 

Laryngol., 72, 507-528. 

1963: Experimental 

I. Directional preAnn. Oto-, Rhino-, 

-22-