1*

positioned at the center of rotation. The rota-
tion schedule comprised: (a) 30 see at a con-
stant velocity of 1 rpm; (b) acceleration; (c)
60 see at a constant velocity of 10 rpm; (d)
deceleration to zers velocity, The combination
of CCW threshold accelerations and sub-
threshold decelerations, and irrigation of the
right ear with cool water, was designed to

‘Timit the elicitation of primary nystagmus to a

single direction, ciz., with the fast phase to the
left. Stimulation always began within 10 sec
of the onset of total darkness, Rest intervals of
12-15 minutes separated trials,

Data from 6 of 10 cats are presented here.
The fotn discarded records were due to: (a) in-
terruption of recording hy loss of electrode
contact (1 animal); (b) responses to the pre-
test or to the first irrigation were too poor to
be quantified (3 animals), To obtain further
data from the same sct of 6 animals, additional
trials were conducted following the post-test.
Two animals cach were stimulated with: (a)
warm water (53.5° C) in the untested (left)
car (to clicit nystagmus in the same direction
as that occasioned during habituation); (b)
warm water (535° C) in the tested (right)
ear; (c) cool water (23.5° C) in the untested

(teft) car. The latter two conditions each pro-
duced nystagmus in the opposite direction from
that-clicited during the habituation trials, Thus
the question of directional transfer could also
be examined, A procedural outline appears
in Table 1,

RESULTS

Measurements of slow-phase displacement,
frequency, and duration of nystagmus were
obtained from cach animal, Scoring for the
primary response began with the onset of
acceleration in the pre- and post-tests, and with
the termination of irrigation in the caloric series.
Secondary nystagmus (a nystagmus which fol-
fows and beats in a direction opposite to that
of a declining primary response, in the apparent
absence of * hysteal stimulation) was scored
from the point of its onset.

Examples of recorded nystagmus responses
appear in Figure 1. A clear decline in the vigor
of the caloric reaction as a result of repeated
elicitation Is evident for both of the animals
represented, The post-test acceleration records
show only minor changes from the pretest:
durations for primary responses are somewhat
shorter, the beats seem more regular and the

TABLE 1
THE PROCEDURAL CONDITIONS EMPLOYED
No, of Fast-Phase
Cats, Trfale = Teale Conditions Direction
All". Pretest 1 4.15*/see’ CCW accel Left
| for 13 sec; sub-threshold decel
i 4
All Habituation 15 23.5° C water to right Left
" 2 5 ear for 30 sec
Al’ Port teay/ 1 418*/sec* CONV accel Left
an, for.13 see; substhreshold decel
1&2 Directional 1 533° C water to left Left
transfer ‘ ear for 30 sec
3&4 Directional’ =f 83.5° C water to right Right
* transfer ear for 30 sec
$&6 Directional 1 233° C water to left . Right
transfer ear for 30 see

-2-


Figures 5 and 6 contain slow-phase displace-
ment and beat-frequency curves obtained by
stimulating the right ear with warm water,
or the left ear with either warm or cool water.
These trials were conducted after the post-test
rotations. The data clearly indicate that uni-
lateral caloric habituation is specific to the
direction elicited during habituating trials.

Secondary nystagmus data are plotted in
Figures 7 and 8, The caloric secondary Is
extremely irregular in early trials, but shows

=a definite decline with repeated elicitation

(Figure 7). The pre- and post-test (rotation)
secondary shows very little change, The one

tion Is an increase of one-fourth to one-
third in duration of the post-test response

(Figure 8),

DISCUSSION

Primary Nystagmus. Repeated unilateral ca-
loric irrigation of the cat in total darkness
results in a marked decline In slow-phase
displacement, frequency, and duration of
vestibular nystagmus, These findings aro in
agreement with caloric data obtained by Hen-
riksson et al, (1962) under conditions of illu-
mination and with results reported by others
(Collins, 1963; Crampton, 1961, 1962; Cramp-
ton & Schwam, 1961) for repeated rotational
stimulation. The greatest amount of decline
occurs during the first 5 trials (Figure 3), This
closely parallels the manner in which rotation-
induced primary nystagmus habituates (Collins,
1963b). i

“Transfer of Hbituation \

Stimulus transfer, The pre- and post-test
rotation data (Figure 4) shasv a general, but
small decline effected by tho/Intervening calor.
lzations, Of the 3: measures, duration of
response ts least affected, while the total fre-
quency and the total slow-phase alisplacement
are reduced by approximately one-third (Fig-
ute 3), This amount of decline ts exceedingly
small considering the marked alteration In re
sponse to the 18 caloric trials and ts equivalent
to what might be obtained as a result of only
3 or 4 consecutive rotations (Collins, 1963b).

Perhaps one of the most significant aspects of
the pre- and post-test graphs fs the fact that
the nystagmus, in both cases, shows no decline
during the 3-sec period after termination of
acceleration. Other data (Collins, 1963b) have
indicated that this holds true for only about 4
consecutive trials at this identical stimulus level,
With the fifth trial, the response has been
shown to drop off sharply from the point of
stimulus termination. Thus, the intervening
caloric trials, although producing a striking
reduction in nystagmus to unilateral irrigation,
exercise relatively little effect on responses to
rotation.

The question of stimulus transfer in ves-
tibular habituation has received little examina-
tion. Maxwell, Burke, and Reston (1922) and
Hood and Pfaltz (1954) habituated rabbits to
rotational stimull and then found “normal”
responses to caloric Irrigation, The former,
however, employed no pre-rotation control trial
and reported no quantified data while Hood
and Pfaltz (1954) based their conclusions pri-
marily upon duration measures, More recently,
Collin¢(196%b) obtained only minor pre- to
posttest caloric changes from the cat after

abituation to rotation, It should be noted
that, in all of these cases, there were apparently
considerable differences in the intensities of
the habituating and transfer stimuli,

Dunlap (1925) employed conditions some.
what more similar to those reported here.
Working with rabbits, he completely abolished
nystagmus to unilateral Ice-water caloric Irriga.
tion first to one ear, and then the other. After
this extensive habituation, responses to rotation
wére absent.

Tt has been suggested that differences In the
relative intensity of rotatory vs. caloric stimula
tlongmafaht have been one cause for the failurr
to obtain transfer of habituation from rotatior
to the caloric situation (Collins, 1963b), The
importance of this Intensity variable for dif
ferences within a stimulus modality has ‘beer
noted (Griffith, 1920; Guedry, 1953, Maxwell
Burke & Reston, 1922), but has not receiver
intensive investigation, It appears that, afte
habituation to a given level of stimulation, 1
more Intense stimulus may evoke a bris!
rexponse,

=8-


secondary nystagmus begins somewhat earlier.

Slow-phase and frequency plots against time
were made for caloric trials 1, 5, 10, and 15
(Figure 2). They indicate that: (a) a con-
siderable overall reduction has occurred within
the first 5 trials; (b) additional stimulation re-
sults in a further overall reduction of the
response, :

Total response-per-trial méasures appear in
Figure 3. A decline in all aspects of the re-
sponse (frequency, slow-phase activity, and
duration) is evident for both the caloric and
rotatory data. The decline in caloric reactivity

WALRISE WARBLER OF WYSTASMIC BEATS
POR 3-SEC. INTERVALS

is marked, although less regular than the fun
tion obtained for rotation (Collins, 1963b
Duration of the rotation-induced nystagmus
only slightly reduced and the drops in fr
quency and a slow-phase displacement are E
factors of about one-third,

The time-course of the responses tu rotatic
are plotted in Figure 4, The nystagmus declir
affects the entire response curve, showing
small, overall depression of ocular activit
For both the pre- and pant-tests, the nystagm:
continues to build up for a see period aft
stimulus termination,

eTmuus 417 sec! fon 13 SEC.

ok oe PRE Test
: is [ oan POST-TEST
: i A AVERAGE FOR 6 CATS.
i b
s)
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ral
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w
Figure 4. Time-coune plots of pre-and post-test rotation-induced Date were
: ta See intervals with the ev the first see.
plotted ts with ception of the fh show point

of stimulus termination. Note that in all cases the response “overshooty” the

termination of acceleration,

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Figure 7, Average slow-phavw diyplacement, duration, and frequency of weoundary nystagmus
Sarees donitg saececive tale deca te ak dane ot the calor eer
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63-14

NYSTAGMUS RESPONSES
OF THE CAT TO ROTATION

AND TO .
) S DIRECTIONALLY EQUIVALENT
a3 \ a EE AND
-— NON-EQUIVALENT STIMULI
2 @ IN Ss AFTER UNILATERAL CALORIC
| S JATIO}
pa pl PA S HABITUATION
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OKLAHOMA CITY, OKLATIOMA
> ,
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. AUGUST 1963

as


SUMMARY

Six cats were exposed to mild angular ac-
celerations before and after an intervening series
of 15 caloric irrigations, All trails were in total
darkness. Slow-phase displacement of the eyes,
beat-frequency, and duration of nystagmus were
scored, All 3 measures reflected a decline in
both the primary and the secondary caloric mea-
sures, Responses to rotation following the cal-
orle habituation showed almost no change, i.e.,

“there was no apparent stimulus generalization,

Differences in: (a) the patterns of nervous ex-
citation elicited by unilateral and bilateral stim.
ulation; and (b) intensity, were hypothesized
as possible causes for the failure to obtain trans-
fer. Additional unilateral caloric trials con-
firmed reports that the reduction of nystagmus
is specific to the direction elicited during habit-
uation trials.

REFERENCES

Aschan, G, Response to rotatory stimuli in
cee pilots Acta Otolaryngol., 1954, Suppl.

Aschan, G, and Bergstedt, M, The genesis of
nystagmus induced by vestibular

stimull. Acta Soc. Med. Upsal., 1955, 60,
113-122,

Collins, W. E. Inverse caloric nystagmus ob-
tained by unilateral stimulation of the cat, Na-
ture, 1062, 195, 808-800,

‘ .
Collins, W. E, Observations on the elicitation of

and in primary nystagmus from
the cat Py caloric irrigation, Acyo-
space Med., 1963 (in Press), a

Collins, W. E. Primary, , and caloric
nystagmus of the cat fo habituation to
rotation, CARI Re ‘63-14%, Oklahoma City,
Oklahoma., 1963.(b

Collins, W. E. and Poo, R. H, Amphetamine,
arousal, and human vestibular nystagmus, J.
Phagnacol, exper. Therap, 1962, 138, 120-125,
Crampton, G, H. Directional imbalance of ves-
tibular nystagmus in cat following repeated
unidirectional angular acceleration, Acta Oto-
laryngol., 1962, 55, 41-48.

@4. ROOVERRMERT FRETTING OFFICE 12.0. TTD

~10-

Crampton, G. H. Effects of visual experience on
vestibular nystagmus habituation the cat, Acta
Otolaryngol., 1962, 55, 516-526.b

Crampton, CG. H. Habituation of vestibular
nystagmus in the cat during sustained arousal
produced by d-amphetamine, USAMRL Report
No, 488, Ft, Knox, Ky., 1961,

Crampton, G, H. and Schwam, W, J, Effects of
arousal reaction on nystagmus habituation in the
cat. Amer, J. Physiol., 1961, 200, 20-33,

Dunlap, K. Adaptation of nystagmus to repeated
caloric stimulation. J. Comp. Psychol, 1925, 5,
485-493,

Fluur, E, and Mendel, L, Habituation, effer-
ence and yestibular interplay. 11. Combined
caloric habituation, Acta Otolaryngol. 1962,
55, 136-144,

Griffith, C, R. The organic effects of repeated
bodily rotation. J. exp, Psychol., 1920, 3, 15-47.
Guedry, F, E. The transfer of habituation to
rotation with respect to the magnitude of the
vestibular stimulus, USNSAM Jt, Proj. Report
No, 34, Pensacola, Fla., 1953.

Guedry, F. E. and Kalter, H. Description of a
human rotation device, USAMRL Report No.
242, Ft. Knox, Ky., 1086,

Mauty, G. T. and Wendt, G. R, Secondary ocu-
lar nystagmus as a function of Intensity and
duration of acceleration, SAM Report 60-29,
Brooks AFB, Texas, 1960,

Henriksson, N, G., Fernandez, C., and Kohut,
R, The caloric test in the cat, Acta Otolaryngol.,
1961, 53, 21-3,

Henriksson, H. G., Kohut, R., and Fernandez,
C. Studies on habituation of vestibular reflexes.
I. Effect of repetitive caloric test. Acta Oto-
laryngol, 1961, 83, 333-249,

Hoods Jy D. and Pfaltz, C, R. Observations up-
on the, effects of repeated stimulation upon
rotational and caloric nystagmus, J, Physiol.
19054, 124, 130-144.

Maxwell, S, S,, Burke, V. C., and Reston, C, R.
Tho effect of repeated rotation on the duration
of aftersnystagmus in the rabbit. Amer, J, Phy-
slol., 1928, 58, 432-438,

Wendt, G. R. Vestibular functions, In S, S.
Stevens (Ed.), Handbook of Experimental Psy-
chology, N. Y.: Wiley, 1951, pp, 1191-1223,


A second factor has also been suggested to
account for the failure to obtain positive results
fri transfer tests (Collins, 1963b), Data ob-
tained here lend some support to Its possible
importance. In the present study, the initial
caloric nystagmus output exceeded the rotation
sesponse by a considerable amount, Thus the
animals were habituated to a stimulus which
was Initially more intense than that experienced
during the pre- and post-tests, This intensity
difference would appear to favor a*transfer
effect. That such transfer did not occur might
be accounted for by differences in the neural
excitation patterns generated by unilateral and
bilateral stimulation. That is, the habituating
mechanism may respond with a relative spe-
cificity that is related to whether a single
horizontal semi-circular canal is stimulated re-
petitively, or whether both canals are simultan-
eously activated,

The two explanatory factors outlined above
are not, of course, mutually exclusive, Further

tation Is required to determine the
relative weight of their contributions, — ~

Response transfer, Henriksson et al. (1962)
have presented data which show that unilateral
calorie nystagmus habituation is specific to the
direction of the response elicited during the
habituating trials, Data obtained in this study
(Figures 3 and 6) provide confirmation of
their findings. Thus, after a specific direction
of nystagmus has been habitudted by repeated
unilateral irtigations, a stimulus, applied to the
opposite ear, which drives the response [n the
same direction as that of the habituating trials,
shows a marked depression of reaction, On the
other hand, stimuli'applied unilaterally to either

ear, whi.h provoke a response th the direction -

opposite that of the habituating trials, result
in a vigorous nystagmus, Crampton (1962a)
has presented data which indicate. a similar
directional specificity of cat nystagmus habit.
uated 8 rotation and Aschan (1054) has noted
a relationship between directional preponders
ance of nystagmus in fighter pilots and their
choice of direction in “rolling” their aircraft,

Secondary Nystagmus. Only a few studies
have been concemed with characteristics of
secondary nystagmus (e.g., Aschan & Bergstedt,
1954; Collins, 1962, 1963a,b; Collins & Poe,
1962; Fluur & Mendel, 1962; Hauty & Wendt,
1960), In the cat, the secondary reaction to
rotation has been reported to rise, peak, de-
cline, and habituate In a manner highly similar
to the primary response (Collins, 1963b), In
addition, the slow-phase rotation-induced out-
put of secondary activity in the cat appears
to be‘about one-fourth to one-fifth that of the
primary (Collins, 1963b); for man, the factor
was reported to be about one-half for 3 selected
subjects (Hauty & Wendt, 1960). Some of this
Inter-species difference may be due to more
sustained high levels of arousal in man (Collins
& Poe, 1962; Crampton, 1961; Crampton &
Schwam, 1961) or to the selection of the
human subjects.

In the present study, no consistent relation-
ship between primary and secondary output to
the caloric stimulation can be readily expressed.
That the secondary declines Is clear. The de-
clino, however, ts abrupt after trial 5 (Figure 7)
and quite irregular. During the first 5 trials,
secondary nystagmus alternately declines mark.
edly and returns to its initial level,

All of the animals gave secondary responses
to the pre- and post-test rotation trials and to
tho first caloric irrigation, Thereafter, however,
the number of cats producing secondary re-
sponses varied from } to 5 for trials 2 through 7
= no secondary responses were recorded during
trial 8 — and, similarly, from 1 to 5 for trials
9 through 15, Its appearance in a given animal
is thus not consistent,

No stviking overall change in slow-phase dis-
placement or frequency occurred in the pre-
to post-test comparisons of secondary nystag-
mus, Duration of the response increased,
however, during the post-test (Figure 8).
Parenthetically, it might be added that the tests
employing equivalent (53.5* C to the left car)
and non-equivalent (35° C to the right car
and 238° C to the left ear) stimult showed
only a few scattered beats of secondary

Tesponses.



Figure 5. Directional spreificity of the calorie reponse decline In slow-phasa ou A
directionally cquivalent calorie stimulus applicd to the te car, alter the
series of habituating trials, produces a 1 similar to the last habituation trial
(upper left graph, 1 and 2). Calorle atrmull which elicit nystagmus in the
direction te that of the habituation series produce vigoruus responses
(upper right graph, Cats 3 and 4, and lower left graph, Cats 8 and 6).

7

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_*

" NYSTAGMUS RESPONSES OF THE CAT TO ROTATION AND TO
DIRECTIONALLY EQUIVALENT AND NON-EQUIVALENT STIMULI
AFTER UNILATERAL CALORIC YIABITUATION’

WILLIAM E. COLLINS, Px.D.

CIVIL AEROMEDICAL RESEARCH INSTITUTE,
FAA, OKLAHOMA CITY, OKLAHOMA ~

Cats have demonstrated a decline (“habitua-
tion”) In the nystagmic response to repeated
unilateral calorie irrigation in illumination
(Henriksson, Fernandez, & Kohut, 1961; Hen-
riksson, Kohut, & Fernandez, 1962), to repeated
rotation {n total darkness (Collins, 1963b;
Crampton, 1961, 1962a; Crampton & Schwam,
1961), and to rotation with concommitant
optokinetic stimulation (Crampton, 1962b).
Further, if the clicited nystagmus is limited to
a single direction during the habituating trials,
there appears to be no transfer of the response
decline to vestibularly-induced eye-movements

in the opposite direction (Crampton, '1962a; ”

Henriksson, et al., 1962).

The question of transfer involves stimulus
modality as well as directional effects, Working
with rabbits, Maxwell, Burke, and Reston
(1922) and Hood and Pfaltz (1954) reported
habituation of rotation-induced nystagmus, but
normal responses from the unilateral caloric
irrigations which followed tHe rotatory trials.
Collins (1963b) feund little transfer in the cat;
the frequency of thesbeats to caloric stimulation
was reduced by about one-third after an intet-
vening series of 15 rotations, Dunlap (1925)
obtained a marked stimulus transfer by abolish.
Ing nystagmus through calori¢ irrigation of
the canals first on one ‘side Of the heads of
rabbits, and then on the other, He obtained
ho nystagmus to rotational stimuli after these

treatments. ,

"Data Bitlected with the technical assistance of Kenneth

©, Swain while the author was at the US. Army Meth
cal Rewarch Laboraury, Fort Knas, Ky. asistance
of Jowph BS. Duchon and) Mary Jarre, Carpe in the
provers of date reduction is gratedully acknowhed ged.

The present study was designed to examine,
with cats: (a) the question of transfer of
caloric nystagmus habituation to the rotational
situation: (b) the manner in which caloric
habituation occurs in total darkness; (c) the
effects of stimulus repetition upon the second-
ary nystagmus.

METHODS

Apparatus. Stimulating, restraint, and_re-
cording equipment were identical to those
reported elsewhere (Collins, 1963b). The
rotatory device, described by Guedry and Kal-
ter (1956), was situated in a light-proof room,

“All testing, including calorie irrigation, was

conducted with the animal positioned on the
tumtable. Restraint was effected according to
the technique of Henriksson et al, (1961),

The recording device, an Offner Type T
Electroencephalograph, employed a 1.4 see RC
time constant in amplification, Needle elec
trodes were positioned by the outer canthi for
the recording of horizontal components of ny-
stagmus, An indifferent elect was located
on the crown near the mid-line of the skull.
Signals were led to a terminal box, through
slip-rings, to the recorder located in an adjoin-
ing room,

Procedure. The test room was in total dark-
ness during all trials, The habituation series
consisted of 15 consecutive caloric irrigations of
the right ear of each animal, Water temper
ature: was kept at 23.5° C (+ 0.5° C), The
tests of transfer (pre- and post-tests) consisted
of above-th CCW accelerations (4.15°/
sec! for 13 sec) and sub-threshold decelerations
(0.18°/sec® for 333 sec) with the animal's head

-1-


1*

NYSTAGMUS RESPONSES OF THE CAT
TO ROTATION AND TO
DIRECTIONALLY EQUIVALENT AND
NON-EQUIVALENT STIMULI AFTER
UNILATERAL CALORIC HABITUATION

WILLIAM E. COLLINS, Ph.D.

Chief, Sensory Integration Section
Paychology Branch

,

FEDERAL AVIATION AGENCY
AVIATION MEDICAL SERVICE
AEROMEDICAL RESEARCH DIVISION
CIVIL AEROMEDICAL RESEARCH INSTITUTE
OKLAHOMA CITY, OKLAHOMA

AUGUST: 1963


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