Neuroscience Letters, 22 (1981) 239-244 239 © Elsevier/North-Holland Scientific Publishers Ltd.

N E U R O N S IN T H E POSTERIOR PARIETAL ASSOCIATION CORTEX OF T H E M O N K E Y A C T I V A T E D D U R I N G O P T O K I N E T I C S T I M U L A T I O N

KENJI KAWANO and MITSUYOSHI SASAKI

Department of Neurophysiology, Institute of, Brain Research, School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113 (Japan)

(Received December 12th, 1980; Revised version received December 27th, 1980; Accepted December 27th, 1980)

Single unit recordings were made in the posterior parietal association cortex (area 7) of the behaving monkey during optokinetic stimulation. A class of neurons which responded only to optokinetic stimulation but did not respond to smooth pursuit eye movement in the dark was found and named optokinetic neurons. During optokinetic stimulation, they were modulated even when optokinetic nystagmus was suppressed. They were not modulated during optokinetic after-nystagmus and did not respond to vestibular stimulation. The results suggest that optokinetic neurons in area 7 are likely to provide an information of movement of visual surroundings whether the monkey pursues them or not.

Con t i nuous m o v e m e n t o f the visual su r round ings elicits op tok ine t i c nys tagmus .

D a m a g e to par ie ta l lobe in h u m a n results in i m p a i r m e n t o f op tok ine t i c nys t agmus

[1] with d i m i n u t i o n o f slow phase veloci ty in the d i rec t ion t o w a r d the side o f lesion

[4, 18]. In the monkey , immed ia t e ly af te r the uni la te ra l les ion in the par ie to -

occipi ta l cor tex , ana logous defici ts are obse rved as in h u m a n [9, l l ] . In the

pos te r io r par ie ta l a ssoc ia t ion cor tex o f the monk e y , there have been f o u n d several

classes o f neurons which are ac t iva ted by visual s t imula t ion or dur ing visual ly

gu ided eye movemen t s [6, 9, 10, 12, 15-17 , 21]. A class o f neurons specif ical ly

re la ted w i t h m o v e m e n t o f the visual su r round ings , however , has no t been descr ibed.

The present s tudy has been car r ied out to de te rmine the m o d e o f response o f

neurons in the pos te r io r pa r ie ta l assoc ia t ion cor tex to mov ing visual su r roundings

which can elicit op tok ine t i c nys tagmus .

Single uni t recordings were m a d e in a rea 7 o f two hemispheres o f the awake

rhesus monkey , using g lass -coa ted Elg i loy e lect rodes . H o r i z o n t a l eye movement s

were recorded as DC e l ec t roocu log ram (EOG) with A g - A g C l e lec t rodes chronica l ly

imp lan ted on the ou te r canthus o f each eye. A ver t ica l ly s t r iped cyl inder (160 cm in d iamete r , 120 cm in height , a l t e rna t ing 3 ° b lack and 27 ° white str ipes) , which to ta l ly

enclosed bo th the m o n k e y and the chair , was i l l umina ted f rom inside and ro ta ted

s inusoida l ly or at a cons t an t veloci ty a r o u n d the s t a t i ona ry an ima l . Op tok ine t i c

nys tagmus was el ici ted by ro t a t ion o f the cyl inder , i .e. op tok ine t i c s t imula t ion . As

240

in a previous paper [7], the animal was seated in a primate chair that could be oscillated about the vertical axis for vestibular stimulation. The animal 's head was fixed to the chair in its normal upright position and the center of the head was placed on the axis o f rotation of the chair and the cylinder. The monkey was trained, in advance, on a visual fixation task according to the method of Wurtz [20]. The animal was first required to look at a small light and to push the lever when the light brightened. Then, the animal was required to fixate the light for 2 -10 sec and to release the lever as soon as the light dimmed. When the target light was attached to the rotating cylinder, the monkey made smooth pursuit eye movements. Then, in order to suppress the optokinetic nystagmus, the target was fixed at the level of the animal 's eye on the floor independent of the rotating cylinder. The unit activities during each task were averaged by a PDP 11/03 computer. A time histogram of spike occurrences was constructed and displayed on a VT 55 terminal. The spike occurrences and movements of the eye, chair and cylinder were monitored on oscilloscopes and on a mingograph.

Sixty-three neurons, which were recorded in the anterior bank of superior temporal sulcus in the posterior part of area 7, were modulated during optokinetic stimulation. Thirty-eight of them were excited by rotation of the striped cylinder to the ipsilateral side, and were suppressed by rotation to the opposite direction. The remaining 25 neurons were excited during optokinetic stimulation directed to the contralateral side and were suppressed during optokinetic stimulation to the ipsilateral side.

Among the neurons which were modulated during optokinetic stimulation, 23 neurons were tested with visual tracking in the dark room. Eight of the 23 neurons were modulated during smooth pursuit eye movement as well, and were therefore classified as visual tracking neurons [10, 12, 16]. The remaining 15 neurons did not respond to smooth pursuit eye movement , but responded only to optokinetic stimulation. The latter class of neurons will be called 'optokinetic neurons ' .

Fig. 1 shows the responses of an optokinetic neuron, recorded in area 7 of the right hemisphere, during optokinetic stimulation. In Fig. 1A, the cylinder was lit and rotated sinusoidally. When the cylinder moved from the ipsilateral to the contralateral side, optokinetic nystagmus, slow phase to the contralateral side, was elicited and the firing rate of the neuron increased. When the cylinder moved from the contralateral to the ipsilateral side, optokinetic nystagmus, slow phase to the ipsilateral side, was elicited and the firing rate of the neuron decreased. Fig. 1B and C show the activities of the same neuron during rotation of the cylinder at a constant velocity. In B, the cylinder was rotated from the ipsilateral to the contralateral side at 90°/sec. When the cylinder was lighted, optokinetic nystagmus was elicited and the neuron showed a striking increase in discharge frequency. When the light was turned off , the firing rate of the neuron immediately decreased to the spontaneous level, although nystagmus continued as optokinetic afternystagmus and then gradually diminished. In C, the cylinder was rotated in the opposite

241

A 6O

i ~ IO(] 4

~ 50 0 2 4 6 B tO SEC

I B I l l II I B I ] I I II L

V ° H EOG

R U l l I I I|1 B i l l III III H EOG

"~ \~- . - - ' / _ " ~ N ~"

BIDBI I l i l l l III I

L

R

B

2'0 £0 60 80 $EC

,~ ~3o.

C

0 20 4'0 60 80 SEC

ON OFF

Fig. 1. Responses of an optokinetic neuron in area 7 of the right hemisphere. A: neural activity during sinusoidal rotation of the lighted cylinder around the monkey. Records, from top to bottom, indicate the averaged histogram of spike occurrences, three pairs of impulse raster and horizontal EOG, and the position of the cylinder. B and C: responses of the same neuron during rotation of the cylinder at a constant velocity. B: rotation from the ipsilateral to the contralateral side at 90°/sec. C: rotation from the contralateral to the ipsilateral side at 30°/sec. The cylinder was lit for 20 sec (between two dotted lines) in each case. Records, from top to bottom, indicate neuronal activity (running average over 800 msec) and horizontal EOG. Note that the neuron showed modulation of firing rate during optokinetic nystagmus and not during optokinetic after-nystagmus. Upward deflections of eye and cylinder signals denote movements to the left side (contralateral side).

direct ion at 30°/sec, and the activity of the n e u r o n was suppressed when the

cylinder was lighted. On the other hand , the neu ron did not respond at all when the

an imal pursued a mov ing target in the dark (Fig. 2A).

Vest ibular nucleus neurons change their discharge rate in response to optokinet ic

s t imula t ion [5]. Thei r response to optokinet ic s t imula t ion cont inues during

optokinet ic af ter -nystagmus, when the movemen t of the visual sur roundings cannot

be seen [19]. However, the optokinet ic neuron in Fig. IB and C showed modu la t i on

of the firing rate only dur ing optokinet ic nys tagmus, and not dur ing optokinet ic

af ter -nystagmus. The same neu ron was not modula ted by sinusoidal ro ta t ion of the

chair in complete darkness. These results indicate that this neuron did not receive

vest ibular input and the response of this n e u r o n to optokinet ic s t imula t ion was not

mediated by the vest ibular nuclei.

Discharge rates of 4 optokinet ic neurons in area 7 examined dur ing optokinet ic

242

H EOG

TARGET

CYLINDER

A 80-

0 0 : : f2 ~ 6 o ~t~o SEC

! KD KU LI

B

J

L] L

I' 30"

R

30"

R

Fig. 2. Responses of the same neuron as Fig. 1. A: during smooth pursuit eye movement in the dark. B: during suppression of optokinetic nystagmus. Records, from top to bottom, indicate the averaged histogram of spike occurrences, horizontal EOG, position of the target and that of the cylinder. Upward deflections of eye, target and cylinder signals denote movements to the left side (contralateral side). El, onset of the target light; KD, closure of the signal key; KU, key release at the arrow.

a f t e r -nys t agmus were a lmos t equal to the spon taneous level. Five op tok ine t i c

neurons were tested by s inusoida l ro ta t ion o f the chair in comple te darkness . None

o f them were m o d u l a t e d by such ves t ibular s t imula t ion . Thus , the op tok ine t i c

neurons are unl ikely to receive input f rom the ves t ibular system.

In o rder to know whether the op tok ine t i c neuron responds to movemen t o f visual

su r round ings dur ing suppress ion o f eye movemen t , the fo l lowing exper iment was

carr ied out on the same neuron . The m o n k e y was requi red to f ixate on the

s t a t ionary target dur ing s inusoidal ro t a t ion o f the s t r iped cyl inder (Fig. 2B).

Optok ine t i c nys tagmus was suppressed in this s i tua t ion , while the firing ra te o f the

neuron was m o d u l a t e d in the same way as in the non- f ixa t ing condi t ion . Its act ivi ty

increased dur ing ro t a t ion o f the cyl inder to the con t ra l a t e ra l side and decreased

dur ing ro t a t ion to the ips i la tera l side. Thus , the neuron r e sponded to m o v e m e n t o f

the visual su r round ings wi thout concomi t an t eye movemen t . Al l 23 op tok ine t i c

neurons r e sponded dur ing suppress ion o f op tok ine t i c nys tagmus .

Op tok ine t i c neurons were f o u n d to be specif ical ly cor re la ted with movemen t o f

visual sur roundings . M o v e m e n t o f the visual su r round ings can be perceived whether

op tok ine t i c nys tagmus is el ici ted or suppressed . As a poss ib le func t ion o f

op tok ine t i c neurons , their ac t iv i ty is p r o b a b l y re la ted with the percep t ion o f the

243

moving visual surroundings. On the other hand, as previously mentioned, lesions in the parieto-occipital cortex result in impairment of optokinetic nystagmus [1, 4, 9, 11, 18]. Efferent projections from area 7 reach the pretectum [8, 13], which is considered to be a crucial link in the afferent path of the optokinetic system [2, 3, 14]. It seems likely, therefore, that an information of moving surroundings provided by optokinetic neurons descends to the brain stem and serves to keep an appropriate function of the optokinetic system.

We thank Dr. H. Sakata for his valuable advice throughout the course of experiments and many useful comments in preparing the manuscript, and Prof. H. Shimazu for his constant encouragement. We express our thanks to Mrs. K. Katagiri for her secretarial assistance, and to Miss C. Utena for her assistance in histology.

1 Carmichael, E.A., Dix, M.R. and Hallpike, C.S., Lesions of the cerebral hemispheres and their effects upon optokinetic and caloric nystagmus, Brain, 77 (1954) 345-372.

2 Cazin, L., Precht, W. and Lannou, J., Pathways mediating optokinetic responses of vestibular nucleus neurons in the rat, PflOgers Arch., 384 (1980) 19-29.

3 Collewijn, H., Oculomotor areas in the rabbit's midbrain and pretectum, J. Neurobiol., 6 (1975) 3-22.

4 Cogan, D.G. and Loeb, D.R., Optokinetic response and intracranial lesions, Arch. Neurol. Psychiat., 61 (1949) 183-187.

5 Henn, V., Young, L.R. and Finley, C., Vestibular nucleus units in alert monkeys are also influenced by moving visual fields, Brain Res., 71 (1974) 144-149.

6 Hyv~irinen, J. and Poranen, A., Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys, Brain, 97 (1974) 673-692.

7 Kawano, K., Sasaki, M. and Yamashita, M., Vestibular input to visual tracking neurons in the posterior parietal association cortex of the monkey, Neurosci. Lett., 17 (1980) 55-60.

8 Kuypers, H.G.J.M. and Lawrence, D.G., Cortical projections to the red nucleus and the brain stem in the rhesus monkey, Brain Res., 4 (1967) 151-188.

9 Lynch, J.C., The functional organization of posterior parietal association cortex, Behav. Brain Sci., in press.

10 Lynch, J.C., Mountcastle, V.B., Talbot, W.H. and Yin, T.C.T., Parietal lobe mechanisms for directed visual attention, J. Neurophysiol., 40 (1977) 362-389.

11 McLaren, J.W. and Lynch, J.C., Quantitative studies of optokinetic nystagmus in monkeys before and after lesions of parieto-occipital association cortex, Neurosci. Abstr., 5 (1979) 797.

12 Mountcastle, V.B., Lynch, J.C., Georgopoulos, A., Sakata, H. and Acuna, C., Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space, J. Neurophysiol., 38 (1975) 871-908.

13 Petras, J.M., Connections of the parietal lobe, J. psychiat. Res., 8 (1971) 189 201. 14 Precht, W. and Strata, P., On the pathway mediating optokinetic responses in vestibular nuclear

neurons, Neuroscience, 5 (1980) 777-787. 15 Robinson, D.L., Goldberg, M.E. and Stanton, G.B., Parietal association cortex in the primate:

sensory mechanisms and behavioral modulations, J. Neurophysiol., 41 (1978) 910-932.

244

16 Sakata, H., Shibutani, H. and Kawano, K., Parietal neurons with dual sensitivity to real and induced movements of visual target, Neurosci. Lett., 9 (1978) 165 169.

17 Sakata, H., Shibutani, H. and Kawano, K., Spacial properties of visual fixation neurons in posterior parietal association cortex of the monkey, J. Neurophysiol., 43 (1980) 1654 1672.

18 Smith, J.L. and Cogan, D.G., Optokinetic nystagmus: a test for parietal lobe lesions, Amer. 3. Ophthal., 48 (1959) 187 193.

19 Waespe, W. and Henn, V., Vestibular nuclei activity during optokinetic after-nystagmus (OKAN) in the alert monkey, Exp. Brain Res., 30 (1977) 323-330.

20 Wurtz, R.H., Visual receptive fields of striate cortex neurons in awake monkeys, J. Neurophysiol., 32 (1969) 727-742.

21 Yin, T.C.T. and Mountcastle, V.B., Visual input to the visuomotor mechanisms of the monkey's

parietal lobe, Science, 197 (1977) 1381 1383.