OB,q) as a narrow band of large cells which have been said to 'prouect, the. Recently Myers [1962] has produced new and very clear anatomical evidence

Transcription

1 THE FUNCTION OF THE CALLOSAL CONNECTIONS OF.THE VISUAL CORTEX. By B. P. CHOUDHURY, D. WHITTERIDGE and M. E. WILSON. From the M.R.C. Group for the Study of Central Mechanisms of Vision, Department of Physiology, University of Edinburgh. (Received for publication 31st October 1964) There is anatomical evidence in cats and baboons of cells at the margin of area 17 which have callosal connections to corresponding points in the opposite hemisphere. The function of such a pathway has been studied in cats after one optic tract has been cut. The corresponding hemisphere now gives early visual responses only at the margin of area 17. Such responses can only be elicited by light stimuli near the vertical meridian of the visual field. These responses are abolished by cooling the corresponding points in the opposite hemisphere and by cutting the corpus callosum. This pathway appears to provide some functional union for the two halves of the visual field. IT has been suggested for some time on anatomical and physiological grounds that whilst the striate cortex (area 17 of Brodmann) has no callosal connections, area 18 has such connections in plenty [von Bonin et al., 1942]. Recently Myers [1962] has produced new and very clear anatomical evidence that only area 18 has callosal connections in the monkey and that there are none in areas 17 and 19. In view of the fact that the boundary of area 17 in the monkey is formed almost entirely by the representation of the vertical meridian [Daniel and Whitteridge, 1961] and that the only connections between areas 17 and 18 are quite short [Le Gros Clark, 1941], we have tested the hypothesis that area 18 is concerned with linking together the two halves of the visual field across the vertical meridian which runs through the fixation point. Anatomy There is general agreement that in the monkey and baboon the striate area ends 2-3 mm. behind the lunate sulcus and that area 18 of Brodmann occupies the lip of the sulcus itself. The part of area 18 immediately adjacent to area 17 is described by von Bonin [1942] (who prefers OBg to von Economo's [1929] nomenclature of OB,q) as a narrow band of large cells which have been said to 'prouect, the visual area from the rest of the cortex'. This band is best developed in man, but easily recognizable in the macaque. No separate band of large cells corresponding to OBg can be seen in the cat. The boundary between 18 and 19 is not clearly defined in the monkey [von Bonin, 1942] and probably is still more difficult to define in the cat. In this work we have only been concerned with the part of area 18 which is immediately adjacent to area 17. Area 18 forms a narrow strip which surrounds that part of area 17 which lies in the calcarine fissure. In the work of Myers [1962] a narrow band of 214

2 Visual Callosal Connections 215 degenerating fibres is to be found at the border of the striate region after the opposite occipital pole has been removed. The extreme anterior part of the striate area lies in the calcarine fissure and probably includes a small area for the representation of the extreme peripheral field 900 out. It is possible that this area is not surrounded by area 18. This point could be studied more readily in the cat, in which the extreme periphery has a larger representation. It is to be found on the lateral aspect of the lateral geniculate nucleus [Seneviratne and Whitteridge, unpublished], and though it has not been directly mapped on the cat's cortex, it is likely that it occupies an appreciable length of that part of the boundary of area 17 which lies in the suprasplenial sulcus [Bilge et al., unpublished]. It is this part of the boundary of 17 which is said by Otsuka and Hassler [1962] not to be surrounded by area 18. These authors describe area 18 as a band of appreciable width on the lateral and post lateral gyrus. We agree with them that the area striata ends in this region, and agree also that there is a small amount of individual variation, and that although the greatest part of the area striata is always on the medial wall of the hemisphere, it extends on to the lateral gyrus from nil to a few mm. Callosal connections between the lateral gyri were described by Polyak [1927]. METHODS In ten cats anaesthetized with 80 mg. chloralose/kg. we have cut the left optic tract just behind the chiasma, by an approach through the mouth. The soft palate was split in the midline and the basisphenoid removed till the dura was visible. A Zeiss binocular operation microscope with 9 in. working distance was used for the later experiments. The hole was plugged with periodontal dressing 'Coe-pak'. The visual cortex was then exposed by a hole 1-5 cm. in diameter across the midline. After the dura had been removed up to the edges of the sagittal sinus, the hole was filled with 4 per cent agar with a little gelatin, at 420 C. Stainless steel or tungsten needles, as described by Hubel [1959], were used. In most experiments alcohol circulated through a block of enamelled copper about 5 mm. x 3 mm. used for cooling the right hemisphere. In later experiments a needle cooled by the expansion of propane [Dondey et al., 1962] was used with a shaped metal foot. In both cases cooling below 100 C. but not below 00 C. was effective in producing temporary nerve cell paralysis. The eye was fixed with the pupil vertical by four ligatures in the fornix which tied the eye to a brass ring which could be clamped. The fundus was observed by an indirect ophthalmoscope and a mirror placed at the centre of the perimeter. The eye was then moved until the area centralis occupied the centre of the field of view. In two baboons the bone was removed over the lunate sulcus and behind it to form a slot about 1 cm. wide extending on both sides 5-6 cm. from the midline. The optic tract was not cut. Strychnine 1 per cent was applied by blotting paper to one hemisphere and responses were obtained from wick electrodes on the opposite hemisphere. RESULTS In the cat the right hemisphere was first mapped to determine the boundary of the left visual field (fig. 1). The electrode was then moved to the left

3 216 Choudhury, Whitteridge and Wilson hemisphere, which was found to be inexcitable by light except for a strip 1-2 mm. wide on the lateral gyrus (fig. 2). The medial surface and the suprasplenial sulcus were explored by needle L FIG. 1. Open circles 0, receptive fields of points in the normal right hemisphere. Filled circles *, receptive fields obtained from the left hemisphere. The broken line indicates the vertical meridian of the right eye. There had been an error of about 100 in its fixation. tracks 1-2 mm. from the midline and carried 6-7 mm. deep. In all experiments in which the optic tract was found to have been completely cut, no visual responses were obtained from any part of the primary visual area, nor from that part of the lateral gyrus which forms part of visual II. Between the two lay the active area which we identify as the medial edge of area 18. The receptive fields were found to be within a few degrees of the vertical meridian (fig. 1). We cannot exclude the possibility of some crossed activity in the lateral sulcus several millimetres lateral to visual II, and we have evidence of late responses in the suprasylvian region. Responses

4 Visual Callosal Connections 217 could be elicited from the near neighbourhood of the vertical meridian in either eye. Responses in area 18 of the left hemisphere were reversibly abolished by cooling corresponding points in the right hemisphere below 100 C. This was a localized effect, and cooling an area 3 mm. in front of the corresponding point had no effect. Complete section of the corpus callosum abolished the effect permanently. It was twice abolished, once only temporarily, by A 10 A * * A FIG. 2. A plot of electrode positions on the left A 4 and right hemispheres. IAP intra aural plane. Ordinate stereotaxic planes, abscissa mm. to left and to right of midline. These points had receptive fields indicated in fig A 2 IAP + + O *.- P2 P4 L R electrolytic lesions in the posterior part of the corpus callosum and once was reversibly abolished by a needle cooled at its tip by the expansion of propane. The needle tip was pushed down between the hemispheres so that its foot lay on the splenium of the corpus callosum. Six single units were obtained in which the receptive field could be plotted. They all fell into the category of cells with simple fields [Hubel and Wiesel, 1962] and had band-shaped receptive fields orientated obliquely to the horizontal. Cooling of the corresponding point in the opposite cortex abolished their activity. The latencies of responses in the right hemisphere to small flashes were msec. and no consistent increase in latency was detected in the left hemisphere. In some experiments the response decayed sooner in the left hemisphere if the flash repetition rate was raised from 1/sec. to 3-4/sec., a rate which had no effect at least on the earliest response in the normal hemisphere.

5 218 Choudhury, Whitteridge and Wilson In the baboon, strychninization of a point in area 18 on the right hemisphere gave rise to a strychnine wave when a visual stimulus was within 50 of the vertical meridian. Only about 8-9 of the vertical meridian immediately below the fixation point was available for study. As the point strychninized was moved medially, so the visual stimulus had to be further below the fixation point. This was to be expected from the mapping of Talbot and Marshall [1941] and Daniel and Whitteridge [1961]. Strychnine spikes could be picked up from the corresponding points in the opposite hemisphere. Moving the recording electrode posteriorly away from the corresponding point rapidly attenuated the spike recorded. No transmission across to the opposite hemisphere was seen on strychninizing points more than a few mm. behind the margin of area 17. DIsCUSSION The experiments on the baboon merely add to the previous work of von Bonin et al. [1942] the information that callosal fibres in area 18 are best excited by visual stimuli near the midline. So far we have failed to cut the optic tract in the baboon. From the experiments on cats we conclude that the visual activity in the left hemisphere whose optic tract had been cut, was due to impulses which had reached the right visual area, had probably been relayed to area 18 of that cortex, and had travelled via the corpus callosum to the left hemisphere. The failure to follow a raised rate of stimulation is strongly suggestive of a larger number of synaptic relays. Unfortuniately we cannot yet excite a single unit in one hemisphere via its own lateral geniculate nucleus and determine its receptive fiejd, and then redetermine its receptive field when excited via the corpus callosum, though the development of reversible methods of blocking should make this possible. If this were feasible, we could find if one and the same cell could only be excited by, say, horizontal bars at the edge of the left and the right visual fields. At least the fact that cells excited via the corpus callosum retained a 'band-shaped' receptive field, makes it certain that they receive connections only from cells whose receptive fields are similarly orientated. The simplest hypothesis, then, is that cells of the visual cortex whose receptive fields are closely adjacent to the vertical meridian and are similarly orientated, are linked to each other via areas 18 and the corpus callosum. Presumably this is a mechanism by which lines in one visual field are linked to corresponding lines in the other field. Although there is no doubt of the existence of a histologically distinct area OB-q in man [von Economo, 1929] there have so far been few speculations on its function. The possibility that there might be disturbances of perception due to splitting of the visual field down the vertical meridian and through the fovea has seldom been discussed. However, if a subject observes a large cathode ray tube on which patches of light of irregular outline appear at random in space and time, he sees a 'fountain' arising somewhere near the centre of the tube and spreading out a little to each side of the midline in

6 Visual Callosal Connections 219 the upper part of the field. If the head is rotated about an anteroposterior axis and held rotated, the axis of the fountain also rotates [MacKay, personal communication]. Lanchester [1934] suggested that objects in the vertical meridian show a greater tendency to disappear during steady fixation. We have repeated his observations but they could not be confirmed. If the mechanism suggested by the present work exists, it must be of great importance in man, since it must be involved during the foveal fixation of any object more than 10 in diameter. REFERENCES VON BONIN, G. (1942). 'The striate area of primates', J. comp. Neurol. 77, VON BONIN, G., GAROL, H. W. and MCCULLOCH, W. S. (1942). 'The functional organization of the occipital lobe', Biol. Symp. 7, CLARK, W. E. LE GRos (1941). 'Observations on the association fibre system of the visual cortex and the central representation of the retina', J. Anat. 75, DANIEL, P. M. and WHITTERIDGE, D. (1961). 'The representation of the visual field on the cerebral cortex in monkeys', J. Phy8iol. 159, DONDEY, M., ALBE FESSARD, D. and LE BEAU, J. (1962). 'Premieres applications neurophysiologique d'une methode permettant le blocage electif et r6versible de structures centrales par r6frig6ration localis6e', Electroenceph. clin. Neurophy8iol. 14, VON EcoNoMo, C. (1929). In Cytoarchitectonics of Human Cerebral Cortex. Trans. S. Parker. London: Oxford University Press. HUBEL, D. H. (1959). 'Tungsten microelectrode for recording from single units', Science, 125, HUBEL, D. H. and WIESEL, T. N. (1962). 'Receptive fields, binocular interaction and functional architecture in the cat visual cortex', J. Phy8iol. 160, LANCHESTER, F. W. (1934). 'Discontinuities in the normal field of vision', J. Anat. 68, MAcKAY, D. M. Personal communication. MYERS, R. E. (1962). 'Commissural connections between occipital lobes of the monkey', J. comp. Neurol. 118, OTSUKA, R. and HASSLER, R. (1962). 'Uber Aufbau und Gliederung des corticalen Sehsphare bei der Katze', Arch. f. P8ychiat. 203, POLYAK, S. (1927). J. comp. Neurol. 44, TALBOT, S. A. and MARsHALL, W. H. (1941). 'Physiological studies on neural mechanisms of visual localization and discrimination', Amer. J. Ophthal. 24,