300
Neuroseienee Research, 12 ( 1991 ) 300-3I)6 ,~, 1991 Elsevier Scientific Publishers Ireland, Ltd. 11168-0102/91/$03.511
N E U R E S 00464
Disjunctive eye movement evoked by microstimulation in an extrastriate cortical area of the cat H. T o d a ~, M. T a k a g i z, T. Yoshizawa z and T. B a n d o Departments ~[~" l Physiology and 2 Ophthalmology, Niigata Unicersity School ~>fMedicine, Niigata (Japan) (Received 18 March 1991; Accepted 17 May 1991)
Key words: Extrastriate cortex; Cat; Eye movement: Ocular convergence; Vergence eye movement; Lateral suprasylvian area
SUMMARY Slow disjunctive eye movement similar to ocular convergence was evoked by microstimulation in parts of the lateral suprasylvian area (LSA) in alert cats. A tungsten-in-glass microelectrode was used for stimulation, and eye movement was monitored using the magnetic search coil method. The velocity-versus-amplitude relationship of disjunctive eye movement evoked by microstimulation was comparable to that of ocular convergence evoked by presenting a visual target. It is suggested that the LSA plays a role in controlling convergence eye movement.
The near response of the eye ~0 is a complex reflex consisting of intraocular muscular movements (lens accommodation and pupillary constriction) and an extraocular muscular movement (ocular convergence). Jampel 16 observed that the triad of the near response was evoked by stimulation of the surface of the parieto-occipital cortex in the monkey. However, only a few physiological studies followed his work. We found that changes in the dioptric power of the eye and the size of the pupil were evoked by microstimulation in the lateral suprasylvian area (LSA) 3 7. The LSA is an extrastriate visual area surrounding the middle suprasylvian sulcus (MSs) in the occipital cortex of the cat ~2,20. In this report, we showed that disjunctive eye movement similar to ocular convergence was also evoked by microstimulation of the LSA applied while monitoring eye movement by means of the magnetic search coil method. A part of the preliminary result was reported in abstract form 24 Five alert cats were used. A chamber for microstimulation and 2 bolts for a head holder were implanted in the skull under pentobarbital anesthesia (35 m g / k g ) at least 1 week before the first experiment. In addition, eye coils to monitor the movement of either eye were sutured to the sclera (modified from Judge et al. ~7). Experiments were performed for 4 - 6 h a day, 5 days a week. During experiments, cats lay in a cloth bag with their head restrained by a head holder 23. They were fed frequently with small
Correspondence." Dr. T. Bando, Department of Physiology, Niigata University School of Medicine, Niigata, Niigata 951, Japan.
301 amounts of liver paste. Eye movement was monitored by using the magnetic search coil method 21. In a few experiments done on 2 cats, changes in the dioptric power of the right eye were also monitored by an infrared o p t o m e t e r 2,9,14. The pupil of the right eye was dilated with a few drops of 10% L-phenylephrine hydrochloride. In these experiments, a visual target was moved in depth along the guide rail in front of the animal under computer control to evoke convergence eye movement. The target was a white circle (diameter, 3 cm) in the center of a black square (7 × 7 cm) presented against the white background. A tungsten-in-glass microelectrode was used for recording unit activities of cortical neurons and for intracortical microstimulation. The electrode was penetrated at 30 ° from the vertical in the frontal plane, so that it was advanced in parallel with the MSs. The point of insertion was determined by both the stereotaxic coordinate in reference to a line on the implanted chamber, and the vascular pattern in the surface of the cortex. The medial and lateral banks of the MSs between the anteroposterior stereotaxic coordinates A10 (most rostral) and P2 (most caudal) were m a p p e d by microstimulation with the anteroposterior and mediolateral spacing of 1 mm. Unit activities of cortical neurons were recorded to ascertain that the electrode was advanced in the gray matter and not in the white matter. Stimulation was done in steps of 500 ~ m . At each site, 5 - 1 0 trials of stimulation were done with intervals of 15-45 s. A train of 200 bipolar pulses of 50 /~A or less (intratrain frequency, 300 Hz) was used. Each pulse in the train was a 0.2-ms negative pulse followed by a 0.2-ms positive pulse. Records of horizontal and vertical components of eye movements evoked by microstimulation (for 4 s, i . e . 2 s before the onset of stimulation, and 2 s following it) were stored on line on a hard disk (sampling frequency, 1 kHz) for later analysis. Records of eye movements, the dioptric power of the eye and unit activities were also stored in analog tapes for off-line analysis. The amplitudes of the disjunctive eye movements were measured as differences between horizontal components of left and right eye movements. The velocities of eye movements were calculated by means of the polynominal curve fitting to traces of eye movements. After the experiment, cats were perfused with saline and 10% formalin transcardially. Brains were cut coronally to 50-/xm thickness by means of freezing microtome, and were stained with neutral red. Electrode tracks were reconstructed in the histological sections, referring to the electrolytic lesions made during the experiment. When a target approached the cat along the guide rail in front of it, slow disjunctive eye movement similar to ocular convergence was evoked (Fig. 1A). The target was initially placed at a distance of 96 cm from the animal. It approached the nose of the cat at the speed of 50 c m / s until it reached a point 22 cm from the animal. Disjunctive eye movement followed the onset of target movement in each of the 5 trials, and attained its maximum amplitudes of 5.7 ° - 7 . 1 ° . The velocity of eye movement tended to increase when the target approached. The maximum velocity in each trial was 6.7-14.5 d e g / s in this animal. In another cat, the maximum amplitude of disjunctive eye movement was 3.1°-4.1° when the target approached for the distance of 74 cm, and the maximum velocities were 4.9-6.8 d e g / s e c . The velocities and amplitudes of disjunctive eye movements are shown in Figure 1C (solid stars, pooled data for 2 cats, the mean and SD of the amplitudes, 2 . 8 ° + 1.8 °, and those of the velocities, 5.4 + 3.0 deg/s). The velocities and amplitudes were positively correlated ( P < 0.001, t-test; coefficient of correlation, + 0.85, n = 43) (Fig. 1C). By microstimulation in a part of the LSA, similar slow disjunctive eye movement was evoked. In Figure 1B, 5 responses are superimposed in reference to the time of
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Fig. 1. (A) Eye movements ew&ed by presenting a visual target, and recorded using the magnetic search coil method. From the top to the bottom, changes in the target position (TARGET), horizontal components of right and left eye movements ( H O R I Z O N T A L R and L), the vertical component of left eye movement (VERTICAL L), and differences between horizontal components of left and right eye movements (HORIZ O N T A L L-R). The responses of 5 trials were superimposed in reference to the times when the target started at the far position (a downward arrow). Far, the position of the target at a distance of 96 cm from the nose of the cat; near, the position of the target at a distance of 22 cm from the cat. (B) Eye movements evoked by microstimulation in the lateral suprasylvian area. From the top to the bottom, horizontal components of right and left eye movements, vertical components of right and left eye movements and differences between horizontal components of left and right eye movements. Responses of 5 trials were superimposed in reference to the onset times of stimuli (a downward arrow). (C) Maximum velocities of disjunctive eye movements (ordinate, in d e g / s ) plotted against their amplitudes (abscissa, in degrees). Solid stars, eye movements evoked by presenting a visual target; open circles, eye movements evoked by microstimulation. Regression lines are shown by solid lines (line a, for solid stars, y = 1.42x + 1.37; line b, for open circles, y - 1 . 7 4 x + 1.12). Confidence intervals (95%) for the population regression line of solid stars are shown by broken lines.
stimulation. By microstimulation, the right eye (the first trace) turned to the left, and the left eye (the second trace) turned to the right. Smaller upward movement was also observed. In the fifth trace, the difference between the horizontal components of left and right eyes in each of 5 trials are shown. The threshold current to evoke this movement was 3 0 / z A . The amplitude of disjunctive eye movement was 0.3 ° - 1 . 7 °, and the maximum velocity was 1.6-4.3 d e g / s . The velocities and amplitudes of disjunctive eye movement evoked by microstimulation are shown in Figure 1C (open circles, data from the same 2 cats as those for solid stars, the mean and SD of the amplitudes, 0.8 ° _+ 0.5 °, those of the velocities, 2.5 _+ 1.5 deg/s). The velocities and amplitudes were positively correlated ( P < 0 . 0 0 1 , t-test; correlation coefficient, +0.60, n = 3 9 ) . The position of the eye in the orbit was not controlled during experiments, and therefore microstimulation was done at various positions of the eye. The disjunctive eye movements were evoked independent of the position of the eye. The effective sites to evoke slow disjunctive eye movement of 0.2 ° or larger were located in the medial bank and fundus of the middle suprasylvian sulcus (MSs) and in
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Fig. 2. Effective sites to evoke disjunctive eye movements of 0.2 ° or larger by microstimulation. A coronal section of the rostral occipital cortex is shown in the inset in the upper left corner. A part of the sections, delineated by a square in the inset, at the level of the anteroposterior stereotaxic coordinates P1, AP0 and A1-A10 are shown in the center of the figure. Solid stars, disjunctive eye movements; open stars, disjunctive eye movements, with the amplitudes of right or left eye movements less than 25% of the total amplitudes; solid triangles, slow conjugate eye movements; solid squares, rapid conjugate eye movements; shaded areas, the areas in which microstimulation was done. Ls = lateral sulcus; MSs = middle suprasylvian sulcus.
the lateral bank of the MSs, corresponding to the posteromedial (PMLS) and posterolateral (PLLS) lateral suprasylvian area 20. Pooled data for 5 cats are shown in Figure 2. Convergence eye movement was observed in the alert cat by showing a visual target in relatively natural circumstances using videotape or photographic recording 15,23. Confirming their findings, we found slow symmetrical disjunctive eye movement similar to ocular convergence by presenting a visual target moving in depth. The maximum amplitudes of these disjunctive eye movements ( 7 ° ) roughly attained the expected amplitude, i.e. 8 ° with the interocular distance of 4 cm if the cat fixated the target throughout its movement. However, by repetition of the visual stimuli, the amplitudes of ocular convergence became smaller. They might not keep full attention on the regularly moving target until it reached the nearer position, as was the case in previous studies. The velocities of disjunctive eye movements in this study were 1-15 d e g / s depending on their amplitudes, and were in agreement with those obtained in a previous study 23 The amplitude and velocity of disjunctive eye movement evoked by microstimulation were smaller than those evoked by presenting a visual target, presumably because the number of neurons activated by intracortical microstimulation was much more restricted than the number of neurons activated by visual stimulation. The velocities and amplitudes of the disjunctive eye movements evoked by microstimulation were positively correlated as were those of disjunctive eye movements evoked by visual stimulation. The regression line of the former (Fig. 1C, line b) is included in the confidence intervals for the population regression line of the latter (Fig. 1C, broken lines). Based on these
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Fig. 3. (A) Sample records obtained by microstimulation at the depth of 5 mm (A I ) and 4.5 mm (A 2) from the surface of the medial bank of the MSs in an electrode track penetrated along the sulcus at the stereotaxic coordinate A6 (Track A). From the top to the bottom, horizontal components of the right and left eye movements (HR and HL), vertical component of the right eye movement (VR), difference between horizontal components of left and right eye movements (HL-HR, disjunctive eye movement), and a change in the dioptric power of the right eye. Each trace indicates the average of 5 responses. A downward arrow shows the onset time of stimulation. Note that the change in the dioptric power in A 2 is barely detectable, while prominent eye movement was evoked. The time calibration in A I applies also to A2, B t and B 2. (B) Similar to A, but sample records were obtained at the depth of 4.5 mm (B I) and 3.5 mm (B 2) in an electrode track at A7 in the same animal (Track B). Calibrations in B 2 apply also to A t, A z and B r (C) Amplitudes of disjunctive eye movements (in degrees; open circles for Track A; solid circles for Track B) and changes in the dioptric power (in diopters; open stars for the Track A; solid stars for the Track B) plotted against the depth from the surface of the bank of the MSs. Sample records were taken at the depth indicated by arrows with labels A~, A 2, B I and B 2.
results, it is suggested that disjunctive eye movements evoked by intracortical microstimulation shared a part of the neuronal circuitry responsible for ocular convergence. Vergence eye movement is closely linked with lens accommodation and pupillary constriction in the near response. The dioptric power of the eye increased, and pupillary constriction was evoked by stimulating parts of the PMLS 4,5,7. Neurons related to changes in the dioptric power of the eye were also recorded in the PMLS 1,3,6. In addition, electromyographic changes in both intraocular and extraocular muscles were evoked by stimulating the PMLS t3. Therefore, disjunctive eye movement evoked by stimulating the LSA might be produced secondarily through the link in the near response. In 2 cats, the LSA was mapped by microstimulation monitoring both eye movements and changes in the dioptric power of the eye in one and the same animal. An example is shown in Figure 3. Disjunctive eye movement was evoked by microstimulation in an electrode track in the medial bank of the MSs at the anteroposterior
305 c o o r d i n a t e A6, while c h a n g e s in t h e d i o p t r i c p o w e r o f the eye w e r e small ( A t) o r b a r e l y d e t e c t a b l e (A2). O n t h e o t h e r h a n d , c h a n g e s in the d i o p t r i c p o w e r w e r e p r o m i n e n t (B 1) at A7, while the disjunctive eye m o v e m e n t was c o m p a r a b l e to t h o s e in A t a n d A 2. In B 2, a c h a n g e in t h e d i o p t r i c p o w e r was e v o k e d with small d o w n w a r d eye m o v e m e n t , b u t w i t h o u t disjunctive eye m o v e m e n t . In C, a m p l i t u d e s o f disjunctive eye m o v e m e n t s ( o p e n a n d solid circles) a n d c h a n g e s in t h e d i o p t r i c p o w e r ( o p e n a n d solid stars) a r e p l o t t e d a g a i n s t the d e p t h f r o m t h e surface of t h e cortex. Disjunctive eye m o v e m e n t was e v o k e d by s t i m u l a t i o n in the d e e p e r p a r t s o f the b a n k s o f t h e MSs. S i m i l a r results w e r e also o b t a i n e d in a n o t h e r cat. T h e s e results favor t h e h y p o t h e s i s t h a t disjunctive eye m o v e m e n t a n d lens a c c o m m o d a t i o n w e r e e v o k e d by s t i m u l a t i n g s e p a r a t e p a r t s o f t h e L S A , a l t h o u g h extensive m a p p i n g in the L S A while m o n i t o r i n g b o t h eye m o v e m e n t a n d c h a n g e s in t h e d i o p t r i c p o w e r r e m a i n s to b e d o n e . T h e L S A plays a role in a n a l y z i n g m o t i o n in 3 - d i m e n s i o n a l s p a c e 8,22,25. A g r o u p o f visual n e u r o n s in this a r e a w e r e a c t i v a t e d by c h a n g e s in t h e o c u l a r d i s p a r i t y a n d / o r t a r g e t size 26,27, which w e r e t h e critical cues to e v o k e lens a c c o m m o d a t i o n a n d v e r g e n c e eye m o v e m e n t 10. T h e n t h e L S A p r o v i d e s the n e c e s s a r y visual i n f o r m a t i o n to c o n t r o l v e r g e n c e eye m o v e m e n t . O n t h e o t h e r h a n d , the L S A was r e l a t e d to eye m o v e m e n t s such as s a c c a d e s 18.19,28 a n d o p t o k i n e t i c n y s t a g m u s 11, in a d d i t i o n to v e r g e n c e eye m o v e m e n t , lens a c c o m m o d a t i o n a n d p u p i l l a r y m o v e m e n t . T h e n it is s u g g e s t e d t h a t t h e L S A not only c o n t r i b u t e s to t h e visual p r o c e s s i n g o f m o t i o n in s p a c e b u t also plays a role in p r o c e s s i n g t h e i n f o r m a t i o n for effective c o n t r o l o f eye m o v e m e n t to follow t h e visual t a r g e t s m o v i n g in t h e s p a c e s u r r o u n d i n g t h e animal. ACKNOWLEDGEMENTS W e a r e i n d e b t e d to P r o f e s s o r M. O k a d a in t h e D e p a r t m e n t of L a b o r a t o r y M e d i c i n e for statistical analysis, a n d to K. K u n i h a r a for p h o t o g r a p h i c work. This w o r k was s u p p o r t e d by a G r a n t - i n - A i d for Scientific P r o j e c t s (02770058) f r o m t h e J a p a n e s e M i n i s t r y o f E d u c a t i o n , Science a n d C u l t u r e to H. T o d a , a n d a G r a n t - i n - A i d for S p e c i a l P r o j e c t s (02255207) f r o m the J a p a n e s e M i n i s t r y of E d u c a t i o n , Science a n d C u l t u r e , a n d a g r a n t f r o m t h e B r a i n Science F o u n d a t i o n to T. B a n d o . REFERENCES 1 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat, Brain Res., 225 (1981) 195-199. 2 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Physiological identification of midbrain neurons related to lens accommodation in cats, J. Neurophysiol., 52 (1984) 870-878. 3 Bando, T., Yamamoto, N. and Tsukahara, N., Cortical neurons related to lens accommodation in posterior lateral suprasylvian area in cats, J. Neurophysiol., 52 (1984) 879-891. 4 Bando, T., Pupillary constriction evoked from the posterior medial lateral suprasylvian (PMLS) area in cats, Neurosci. Res., 2 (1985) 472-485. 5 Bando, T., Depressant effect of cooling of the postero-lateral occipital cortex on pupillo-constriction responses evoked from the lateral suprasylvian area in cats, Neurosci. Res., 4 (1987) 316-322. 6 Bando, T., Toda, H. and Awaji, T., Lens accommodation-related and pupil-related units in the lateral suprasylvian area in cats. In T.P. Hicks and G. Benedek (Eds.), Extrageniculostriate Visual Mechanisms, Progress in Brain Research, Vol. 75, Elsevier, Amsterdam, 1988, pp. 231-236. 7 Bando, T., Norita, M., Hirano, T. and Toda, H., Projections of the postero-medial lateral suprasylvian area (PMLS) to cortical area 20 in cats with special reference to pupillary constriction: a physiological and anatomical study, Brain Res., 494 (1989) 369-373. 8 Camarda, R. and Rizzolatti, G., Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat, Brain Res., 101 (1976) 427-443.
306 9 Campbell, F.W. and Robson, J.G., High-speed infrared optometer, J. Opt. Soc. Am., 49 (1959) 268-272. 10 Davson, H., Physiology of the Eye. Churchill Livingstone, Edinburgh, 1972, pp. 397-413. 11 Hamada, T., Neural response to the motion of textures in lateral suprasylvian area of the cat, Behac. Brain Res., 25 (1987) 175-185. 12 Heath, C.J. and Jones, E.G., The anatomical organization of the suprasylvian gyrus of the cat, Ergebn. Anat. Entwickl.-Gesch., 45 (1971) 1-64. 13 Hiraoka, M. and Shimamura, M., The midbrain reticular formation as an integration center for the near response, Neurosci. Res., 7 (1989) 1-12. 14 Hosoba, M., Bando, T. and Tsukahara, N., The cerebellar control of accommodation of the eye in the cat, Brain Res., 153 (1978) 495-505. 15 Hughes, A., Vergence in the cat, Vision Res., 12 (1972) 1961-1994. 16 Jampel, R.S., Convergence, divergence, pupillary reactions and accommodation of the eyes from faradic stimulation of the macaque brain, J. Comp. Neurol., 115 (1960)371-400. 17 Judge, S.J., Richmond, B.J. and Chu, F.C., Implantation of magnetic search coils for measurement of eye position: an improved method, Vision Res., 20 (1980) 535-538. 18 Kennedy, H. and Magnin, M., Saccadic influences on single neuron activity in the medial bank of the cat's suprasylvian sulcus (Clare-Bishop area), Exp. Brain Res., 27 (1977) 315-317. 19 Komatsu, Y., Shibuki, K. and Toyama, K., Eye movement-related activities in cells of the lateral suprasylvian cortex of the cat, Neurosci. Lett., 41 (1983) 271-276. 20 Palmer, L.A., Rosenquist, A.C. and Tusa, R.J., The retinotopic organization of lateral suprasylvian visual areas in the cat, J. Comp. Neurol., 177 (1978) 237-256. 21 Robinson, D.A., A method of measuring eye movement using a scleral search coil in magnetic field, IEEE Trans. Biomed. Eng., BME-10 (1963) 137-145. 22 Spear, P.D. and Baumann, T.P., Receptive-field characteristics of single neurons in the lateral suprasylvian visual area of the cat, J. Neurophysiol., 38 (1975) 1403-1420. 23 Stryker, M. and Blakemore, C., Saccadic and disjunctive eye movements in cats, Vision Res., 12 (1972) 2005 - 2013. 24 Toda, H., Takagi, M., Yoshizawa, T. and Bando, T., Disjunctive eye movement evoked by stimulation of an extrastriate cortex in cats, Jpn. J. Physiol., 40 (1990) $207. 25 Toyama, K. and Kozasa, T., Responses of Clare-Bishop neurons to three-dimensional movement of a light stimulus, Vision Res., 22 (1982) 571-574. 26 Toyama, K., Komatsu, Y. and Kozasa, T., The responsiveness of Clare-Bishop neurons to motion cues for motion stereopsis, Neurosci. Res., 4 (1986) 83-109. 27 Toyama, K., Fujii, K., Kasai, S. and Maeda, K., The responsiveness of Clare-Bishop neurons to size cues for motion stereopsis, Neurosci. Res., 4 (1986) 110-128. 28 Vanni-Mercier, G. and Magnin, M., Retinotopic organization of extra-retinal saccade-related input to the visual cortex in the cat, Exp. Brain Res., 46 (1982) 368-376.
Neuroseienee Research, 12 ( 1991 ) 300-3I)6 ,~, 1991 Elsevier Scientific Publishers Ireland, Ltd. 11168-0102/91/$03.511
N E U R E S 00464
Disjunctive eye movement evoked by microstimulation in an extrastriate cortical area of the cat H. T o d a ~, M. T a k a g i z, T. Yoshizawa z and T. B a n d o Departments ~[~" l Physiology and 2 Ophthalmology, Niigata Unicersity School ~>fMedicine, Niigata (Japan) (Received 18 March 1991; Accepted 17 May 1991)
Key words: Extrastriate cortex; Cat; Eye movement: Ocular convergence; Vergence eye movement; Lateral suprasylvian area
SUMMARY Slow disjunctive eye movement similar to ocular convergence was evoked by microstimulation in parts of the lateral suprasylvian area (LSA) in alert cats. A tungsten-in-glass microelectrode was used for stimulation, and eye movement was monitored using the magnetic search coil method. The velocity-versus-amplitude relationship of disjunctive eye movement evoked by microstimulation was comparable to that of ocular convergence evoked by presenting a visual target. It is suggested that the LSA plays a role in controlling convergence eye movement.
The near response of the eye ~0 is a complex reflex consisting of intraocular muscular movements (lens accommodation and pupillary constriction) and an extraocular muscular movement (ocular convergence). Jampel 16 observed that the triad of the near response was evoked by stimulation of the surface of the parieto-occipital cortex in the monkey. However, only a few physiological studies followed his work. We found that changes in the dioptric power of the eye and the size of the pupil were evoked by microstimulation in the lateral suprasylvian area (LSA) 3 7. The LSA is an extrastriate visual area surrounding the middle suprasylvian sulcus (MSs) in the occipital cortex of the cat ~2,20. In this report, we showed that disjunctive eye movement similar to ocular convergence was also evoked by microstimulation of the LSA applied while monitoring eye movement by means of the magnetic search coil method. A part of the preliminary result was reported in abstract form 24 Five alert cats were used. A chamber for microstimulation and 2 bolts for a head holder were implanted in the skull under pentobarbital anesthesia (35 m g / k g ) at least 1 week before the first experiment. In addition, eye coils to monitor the movement of either eye were sutured to the sclera (modified from Judge et al. ~7). Experiments were performed for 4 - 6 h a day, 5 days a week. During experiments, cats lay in a cloth bag with their head restrained by a head holder 23. They were fed frequently with small
Correspondence." Dr. T. Bando, Department of Physiology, Niigata University School of Medicine, Niigata, Niigata 951, Japan.
301 amounts of liver paste. Eye movement was monitored by using the magnetic search coil method 21. In a few experiments done on 2 cats, changes in the dioptric power of the right eye were also monitored by an infrared o p t o m e t e r 2,9,14. The pupil of the right eye was dilated with a few drops of 10% L-phenylephrine hydrochloride. In these experiments, a visual target was moved in depth along the guide rail in front of the animal under computer control to evoke convergence eye movement. The target was a white circle (diameter, 3 cm) in the center of a black square (7 × 7 cm) presented against the white background. A tungsten-in-glass microelectrode was used for recording unit activities of cortical neurons and for intracortical microstimulation. The electrode was penetrated at 30 ° from the vertical in the frontal plane, so that it was advanced in parallel with the MSs. The point of insertion was determined by both the stereotaxic coordinate in reference to a line on the implanted chamber, and the vascular pattern in the surface of the cortex. The medial and lateral banks of the MSs between the anteroposterior stereotaxic coordinates A10 (most rostral) and P2 (most caudal) were m a p p e d by microstimulation with the anteroposterior and mediolateral spacing of 1 mm. Unit activities of cortical neurons were recorded to ascertain that the electrode was advanced in the gray matter and not in the white matter. Stimulation was done in steps of 500 ~ m . At each site, 5 - 1 0 trials of stimulation were done with intervals of 15-45 s. A train of 200 bipolar pulses of 50 /~A or less (intratrain frequency, 300 Hz) was used. Each pulse in the train was a 0.2-ms negative pulse followed by a 0.2-ms positive pulse. Records of horizontal and vertical components of eye movements evoked by microstimulation (for 4 s, i . e . 2 s before the onset of stimulation, and 2 s following it) were stored on line on a hard disk (sampling frequency, 1 kHz) for later analysis. Records of eye movements, the dioptric power of the eye and unit activities were also stored in analog tapes for off-line analysis. The amplitudes of the disjunctive eye movements were measured as differences between horizontal components of left and right eye movements. The velocities of eye movements were calculated by means of the polynominal curve fitting to traces of eye movements. After the experiment, cats were perfused with saline and 10% formalin transcardially. Brains were cut coronally to 50-/xm thickness by means of freezing microtome, and were stained with neutral red. Electrode tracks were reconstructed in the histological sections, referring to the electrolytic lesions made during the experiment. When a target approached the cat along the guide rail in front of it, slow disjunctive eye movement similar to ocular convergence was evoked (Fig. 1A). The target was initially placed at a distance of 96 cm from the animal. It approached the nose of the cat at the speed of 50 c m / s until it reached a point 22 cm from the animal. Disjunctive eye movement followed the onset of target movement in each of the 5 trials, and attained its maximum amplitudes of 5.7 ° - 7 . 1 ° . The velocity of eye movement tended to increase when the target approached. The maximum velocity in each trial was 6.7-14.5 d e g / s in this animal. In another cat, the maximum amplitude of disjunctive eye movement was 3.1°-4.1° when the target approached for the distance of 74 cm, and the maximum velocities were 4.9-6.8 d e g / s e c . The velocities and amplitudes of disjunctive eye movements are shown in Figure 1C (solid stars, pooled data for 2 cats, the mean and SD of the amplitudes, 2 . 8 ° + 1.8 °, and those of the velocities, 5.4 + 3.0 deg/s). The velocities and amplitudes were positively correlated ( P < 0.001, t-test; coefficient of correlation, + 0.85, n = 43) (Fig. 1C). By microstimulation in a part of the LSA, similar slow disjunctive eye movement was evoked. In Figure 1B, 5 responses are superimposed in reference to the time of
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stimulation. By microstimulation, the right eye (the first trace) turned to the left, and the left eye (the second trace) turned to the right. Smaller upward movement was also observed. In the fifth trace, the difference between the horizontal components of left and right eyes in each of 5 trials are shown. The threshold current to evoke this movement was 3 0 / z A . The amplitude of disjunctive eye movement was 0.3 ° - 1 . 7 °, and the maximum velocity was 1.6-4.3 d e g / s . The velocities and amplitudes of disjunctive eye movement evoked by microstimulation are shown in Figure 1C (open circles, data from the same 2 cats as those for solid stars, the mean and SD of the amplitudes, 0.8 ° _+ 0.5 °, those of the velocities, 2.5 _+ 1.5 deg/s). The velocities and amplitudes were positively correlated ( P < 0 . 0 0 1 , t-test; correlation coefficient, +0.60, n = 3 9 ) . The position of the eye in the orbit was not controlled during experiments, and therefore microstimulation was done at various positions of the eye. The disjunctive eye movements were evoked independent of the position of the eye. The effective sites to evoke slow disjunctive eye movement of 0.2 ° or larger were located in the medial bank and fundus of the middle suprasylvian sulcus (MSs) and in
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the lateral bank of the MSs, corresponding to the posteromedial (PMLS) and posterolateral (PLLS) lateral suprasylvian area 20. Pooled data for 5 cats are shown in Figure 2. Convergence eye movement was observed in the alert cat by showing a visual target in relatively natural circumstances using videotape or photographic recording 15,23. Confirming their findings, we found slow symmetrical disjunctive eye movement similar to ocular convergence by presenting a visual target moving in depth. The maximum amplitudes of these disjunctive eye movements ( 7 ° ) roughly attained the expected amplitude, i.e. 8 ° with the interocular distance of 4 cm if the cat fixated the target throughout its movement. However, by repetition of the visual stimuli, the amplitudes of ocular convergence became smaller. They might not keep full attention on the regularly moving target until it reached the nearer position, as was the case in previous studies. The velocities of disjunctive eye movements in this study were 1-15 d e g / s depending on their amplitudes, and were in agreement with those obtained in a previous study 23 The amplitude and velocity of disjunctive eye movement evoked by microstimulation were smaller than those evoked by presenting a visual target, presumably because the number of neurons activated by intracortical microstimulation was much more restricted than the number of neurons activated by visual stimulation. The velocities and amplitudes of the disjunctive eye movements evoked by microstimulation were positively correlated as were those of disjunctive eye movements evoked by visual stimulation. The regression line of the former (Fig. 1C, line b) is included in the confidence intervals for the population regression line of the latter (Fig. 1C, broken lines). Based on these
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results, it is suggested that disjunctive eye movements evoked by intracortical microstimulation shared a part of the neuronal circuitry responsible for ocular convergence. Vergence eye movement is closely linked with lens accommodation and pupillary constriction in the near response. The dioptric power of the eye increased, and pupillary constriction was evoked by stimulating parts of the PMLS 4,5,7. Neurons related to changes in the dioptric power of the eye were also recorded in the PMLS 1,3,6. In addition, electromyographic changes in both intraocular and extraocular muscles were evoked by stimulating the PMLS t3. Therefore, disjunctive eye movement evoked by stimulating the LSA might be produced secondarily through the link in the near response. In 2 cats, the LSA was mapped by microstimulation monitoring both eye movements and changes in the dioptric power of the eye in one and the same animal. An example is shown in Figure 3. Disjunctive eye movement was evoked by microstimulation in an electrode track in the medial bank of the MSs at the anteroposterior
305 c o o r d i n a t e A6, while c h a n g e s in t h e d i o p t r i c p o w e r o f the eye w e r e small ( A t) o r b a r e l y d e t e c t a b l e (A2). O n t h e o t h e r h a n d , c h a n g e s in the d i o p t r i c p o w e r w e r e p r o m i n e n t (B 1) at A7, while the disjunctive eye m o v e m e n t was c o m p a r a b l e to t h o s e in A t a n d A 2. In B 2, a c h a n g e in t h e d i o p t r i c p o w e r was e v o k e d with small d o w n w a r d eye m o v e m e n t , b u t w i t h o u t disjunctive eye m o v e m e n t . In C, a m p l i t u d e s o f disjunctive eye m o v e m e n t s ( o p e n a n d solid circles) a n d c h a n g e s in t h e d i o p t r i c p o w e r ( o p e n a n d solid stars) a r e p l o t t e d a g a i n s t the d e p t h f r o m t h e surface of t h e cortex. Disjunctive eye m o v e m e n t was e v o k e d by s t i m u l a t i o n in the d e e p e r p a r t s o f the b a n k s o f t h e MSs. S i m i l a r results w e r e also o b t a i n e d in a n o t h e r cat. T h e s e results favor t h e h y p o t h e s i s t h a t disjunctive eye m o v e m e n t a n d lens a c c o m m o d a t i o n w e r e e v o k e d by s t i m u l a t i n g s e p a r a t e p a r t s o f t h e L S A , a l t h o u g h extensive m a p p i n g in the L S A while m o n i t o r i n g b o t h eye m o v e m e n t a n d c h a n g e s in t h e d i o p t r i c p o w e r r e m a i n s to b e d o n e . T h e L S A plays a role in a n a l y z i n g m o t i o n in 3 - d i m e n s i o n a l s p a c e 8,22,25. A g r o u p o f visual n e u r o n s in this a r e a w e r e a c t i v a t e d by c h a n g e s in t h e o c u l a r d i s p a r i t y a n d / o r t a r g e t size 26,27, which w e r e t h e critical cues to e v o k e lens a c c o m m o d a t i o n a n d v e r g e n c e eye m o v e m e n t 10. T h e n t h e L S A p r o v i d e s the n e c e s s a r y visual i n f o r m a t i o n to c o n t r o l v e r g e n c e eye m o v e m e n t . O n t h e o t h e r h a n d , the L S A was r e l a t e d to eye m o v e m e n t s such as s a c c a d e s 18.19,28 a n d o p t o k i n e t i c n y s t a g m u s 11, in a d d i t i o n to v e r g e n c e eye m o v e m e n t , lens a c c o m m o d a t i o n a n d p u p i l l a r y m o v e m e n t . T h e n it is s u g g e s t e d t h a t t h e L S A not only c o n t r i b u t e s to t h e visual p r o c e s s i n g o f m o t i o n in s p a c e b u t also plays a role in p r o c e s s i n g t h e i n f o r m a t i o n for effective c o n t r o l o f eye m o v e m e n t to follow t h e visual t a r g e t s m o v i n g in t h e s p a c e s u r r o u n d i n g t h e animal. ACKNOWLEDGEMENTS W e a r e i n d e b t e d to P r o f e s s o r M. O k a d a in t h e D e p a r t m e n t of L a b o r a t o r y M e d i c i n e for statistical analysis, a n d to K. K u n i h a r a for p h o t o g r a p h i c work. This w o r k was s u p p o r t e d by a G r a n t - i n - A i d for Scientific P r o j e c t s (02770058) f r o m t h e J a p a n e s e M i n i s t r y o f E d u c a t i o n , Science a n d C u l t u r e to H. T o d a , a n d a G r a n t - i n - A i d for S p e c i a l P r o j e c t s (02255207) f r o m the J a p a n e s e M i n i s t r y of E d u c a t i o n , Science a n d C u l t u r e , a n d a g r a n t f r o m t h e B r a i n Science F o u n d a t i o n to T. B a n d o . REFERENCES 1 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat, Brain Res., 225 (1981) 195-199. 2 Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. and Tsukahara, N., Physiological identification of midbrain neurons related to lens accommodation in cats, J. Neurophysiol., 52 (1984) 870-878. 3 Bando, T., Yamamoto, N. and Tsukahara, N., Cortical neurons related to lens accommodation in posterior lateral suprasylvian area in cats, J. Neurophysiol., 52 (1984) 879-891. 4 Bando, T., Pupillary constriction evoked from the posterior medial lateral suprasylvian (PMLS) area in cats, Neurosci. Res., 2 (1985) 472-485. 5 Bando, T., Depressant effect of cooling of the postero-lateral occipital cortex on pupillo-constriction responses evoked from the lateral suprasylvian area in cats, Neurosci. Res., 4 (1987) 316-322. 6 Bando, T., Toda, H. and Awaji, T., Lens accommodation-related and pupil-related units in the lateral suprasylvian area in cats. In T.P. Hicks and G. Benedek (Eds.), Extrageniculostriate Visual Mechanisms, Progress in Brain Research, Vol. 75, Elsevier, Amsterdam, 1988, pp. 231-236. 7 Bando, T., Norita, M., Hirano, T. and Toda, H., Projections of the postero-medial lateral suprasylvian area (PMLS) to cortical area 20 in cats with special reference to pupillary constriction: a physiological and anatomical study, Brain Res., 494 (1989) 369-373. 8 Camarda, R. and Rizzolatti, G., Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat, Brain Res., 101 (1976) 427-443.
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