binocular projection by electrophysiological methods. An account of some METHODS

Transcription

1 THE PROJECTION OF THE BINOCULAR VISUAL FIELD ON THE OPTIC TECTA OF THE FROG. By R. M. GAZE and M. JACOBSON. From the Department of Physiology, University of Edinburgh. (Received for publication 7th February 1962) The projection of the binocular visual field on the optic tecta of Rana temporaria has been. mapped by recording action potentials evoked in the tectum by a spot of light in the visual field. The binocular visual field extends for about 1000 on the horizontal meridian. Only the central region of the binocular field is represented through both eyes on both ipsilateral and contralateral tecta. The binocular field to the left and right of this central region is represented through both eyes on one tectum only: the left side of the field projects through both eyes to the right optic tectum, while the right side of the field projects through both eyes to the left tectum. Corresponding retinal points project to the same tectal locius. THE representation of the retina on the surface of the contralateral optic tectum of the frog was described by Gaze [1958 a] and worked out in greater detail by Jacobson [1962]. During the course of these experiments it was found that a visual stimulus within the binocular part of each visual field would activate not only the contralateral tectum but also the rostral part of the ipsilateral tectum. The present paper describes an investigation of this binocular projection by electrophysiological methods. An account of some of this work has been published [Gaze, 1958 b]. METHODS In each experiment an adult Rana temporaria was anesthetized with ether, the skull was opened by means of a dental drill, the animal was decerebrated by suction or cautery and immobilized with an injection of 02 mg. tubocurarine into the thigh muscles. The frog was then set up for recording at the centre of the arc of an "Aimark" projection perimeter. The arc had a radius of 33 cm. and the visual stimulus was a spot of light thrown onto the inner side of the arc. In these experiments a spot of 1 mm. diameter was used, subtending 410' at the eye. Recording was done in a darkened room and the brightness of the stmnulus was 41 cd/m2. Two methods were chosen for presenting the results. In one the animal faced the perimeter (fig. 1, inset). Thus the entire binocular visual field could be presented on one perimeter chart in the way which has most relevance tq the animal's normal life. In the second method the left eye was centred on the perimeter and the right eye covered or removed. The eye was centred by using the corneal reflection of a spot of light projected from the "fixation point" in the middle of the perimeter arc. The eye was considered to be centred when this corneal reflection was in the middle of the pupil and was accurately superimposed on the fundal reflex. This alignment of the animal (fig. 3) presents the information on the ipsilateral projection in terms of the visual field of one eye. It enables a direct comparison to be made with the more familiar contralateral projection [Jacobson, 1962, figs. 1 and 2]. Action potentials in response to the light stimulus were recorded from the surface of the tectum by tungsten microelectrodes with tip diameters of between 1 and 5,u. The indifferent electrode was a pin through the hindlegs. The potentials were led 273

2 274 Gaze and Jacobson through an amplifying system with a time constant of 2 msec. and were monitored on a loudspeaker and displayed on an oscilloscope. The shutter of the perimeter was operated by hand and the duration of each stimulus flash was approximately sec. The interval between stimuli was 1 sec. or longer. Under these conditions the response consisted of a burst of action potentials from several units. The procedure in an experiment was as follows: the tectum was photographed and an enlargement made at x 50 magnification. A rectangular grid of lines was drawn on the enlargement, the lines being separated from one another bv 1 cm., corresponding to a separation of 0-02 cm. on the tectum. The presence of a vivid melanophore pattern on the tectal surface, together with the grid on the photograph, enabled the microelectrode to be placed accurately at any position on the dorsal surface of the tectum. With the electrode at a determined position on the tectum the position of the stimulus in the visual field was found which evoked the maximali response. This procedure was repeated with the electrode at different positions on the tectum. RESULTS The optic axes of Rana temporaria diverge by approximately The visual field of each eye extends for about 1100 from the optic axis to the nasal periphery of the horizontal meridian (fig. 1). Thus the visual fields of the two eyes overlap by about 100 in the horizontal meridian and an object in this region of the field can be seen with both eyes. Fig. 1 shows the results of an experiment in which the frog was set up facing the perimeter. With the animal's right eye covered, an electrode at position 22 on the right optic tectum recorded a response mediated through the left eye, when the stimulus was at position 22 in the visual field. When the left eye was covered and the right eye uncovered, a response was recorded, mediated now through the right eye, with the electrode at the same position on the tectum and the stimulus at the same position in the visual field. The optimal stimulus position was the same for the two eyes within the limits of accuracy of the method of localization. The same applies to all the positions marked by the symbols A or *. Therefore corresponding retinal points project to the same tectal locus. The electrode positions marked by the symbols A or o on the caudal part of each tectum (fig. 1) could record responses only from a stimulus presented to the contralateral eye, in the appropriate position in the peripheral part of the field temporal to the optic axis. At each of the electrode positions marked by the symbols A or e, a response could be obtained through both eyes, when the stimulus was in the appropriate position. This binocular region extends horizontally on each side of the mid-sagittal plane as far as the optic axis of each eye. It may be seen that the region of the visual field which projects to the right tectum (shown by the symbols A or A) lies largely to the left of the mnid-sagittal plane (vertical meridian, ), while the region of the field projecting to the left tectum (shown by the symbols o or *) lies largely to the right of the mid-sagittal plane. In the central region of the visual field, directly in front of the frog, there is an overlap of the binocular projection to both tecta. For example, in fig. 1, stimulus positions 13 (A) and 44 (A) are at the same position in the visual

3 0. 0R'~ "b s N 'o 6459 t t e o - S I N FE RIOR FIG. 1.-The projection of the binocular visual field to the optic tecta. Upper diagram.-dorsal view of optic tecta showing electrode positions on tectal surface. Lower diagram.-perimeter chart of the visual field showing stimulus positions. The animal was centred on the perimeter as shown in the inset. The perimeter chart covers 1000 outwards from the centre of the field. The projections of the two optic axes on the chart are marked by the letters R and L and are each 550 out from the centre and 150 up from the horizontal. Stimulus positions indicated by A in the left peripheral part of the visual field project through the left eye to the positions on the right tectum shown by the same symbols. Stimulus positions indicated by A in the field project through both eyes to the correspondingly marked positions on the right tectum. Stimulus positions indicated by 0 in the right peripheral part of the visual field project through the right eye to the correspondingly marked positions on the left tectum. Stimulus positions indicated by * project through both eyes to the correspondingly marked positions on the left tectum. The projection of those parts of the visual field temporal to the optic axes (A and 0) is thus purely contralateral and monocular, through the appropriate eye to the opposite tectum. In the central region of the field around the mid-sagittal plane of the animal ( meridian on chart) the positions which project binocularly to right tectum (A) overlap those which project binocularly to left tectum (0). Points within this region of the field (e.g. stimulus positions 1-13 and 37-45) project through both eyes to both tecta. Points within the binocular region of field (black symbols), but outside the area of overlap, project binocularly to the contralateral tectum only (e.g. 59 and 60 in right field project binocularly to left tectum while 22 and 23 project binocularly to right tectum).

4 276 Gaze and Jacobson field. Therefore a stimulus at this position will evoke a response through both eyes at position 13 on the right tectum and through both eyes at position 44 on the left tectum. This was found to be the case for all the electrode positions within the overlapping region, which in this experiment had an extent of some 400 on the horizontal meridian. Having determined the point to point projection of the binocular visual 60 SUPFE R10F FIG. 2.-The co-ordinates of the binocular field on the optic tecta. This diagram was constructed from the results of the experiment illustrated in fig. 1. The extent of the binocular field is indicated by continuous lines on the perimeter chart and on the tecta. That part of the projection shown by dotted lines is monocular-from left field via left eye to right tectum and from right field via right eye to left tectum. The full extent of each monocular projection is not shown. The projection of the horizontal meridian (0-180 ) and that of the vertical meridian ( ) are shown by thick lines on the tectum. field on both tecta, it was possible to construct a map showing the representation of the meridians and parallels of the field on the tecta. This is shown in fig. 2. The centre of the binocular field, directly in front of the frog, is represented at the rostrolateral poles of both tecta. The vrertical meridian projects symmetrically on both tecta, running from the rostrolateral pole towards the midline. Whereas the entire upper half of the vertical meridian, from the centre of the field out to 100, is represented on both tecta, the horizontal meridian is split so that 500 left of the centre of the field is represented on the right tectum and 500 to the right of the centre of the field is represented on the left tectum. The map shown in this diagram is incomplete since we have not been able to determine the projection from the lower half of the visual field to the inaccessible lateral edge of the tectum.

5 Visual Projection in the Frog 277 The fact that a stimulus within the binocular visual field evokes activity in one tectum through both eyes means that each eye projects not only to the contralateral tectum, but also to the rostral part of the ipsilateral tectum. The relationship of this ipsilateral projection to the visual field of one eye is shown in fig. 3 where the animal was set up with its left eye centred on the perimeter and its right eye removed. The stimulus positions 1-24, indicated by the symbol * in the left visual field, evoked responses at the correspondingly numbered positions on the right optic tectum. This projection is simply part of the contralateral projection [Jacobson, 1962], the remainder of which was not mapped in this experiment. Stimulus positions 1-23, indicated by the symbol G, evoked responses at the correspondingly numbered positions on the left (ipsilateral) tectum. There is a region of overlap between the contralateral and ipsilateral stimulus positions in the visual field, which occurs about 600 nasal to the optic axis. This position lies in the mid-sagittal plane of the animal. In this experiment symmetrical electrode positions on the two tecta have been given the same number, and it may be seen that the ipsilateral and contralateral stimulus positions are symmetrically disposed about the mid-sagittal plane of the animal. DISCUSSION The optic chiasma of the frog is reported to be completely crossed [Wlassak, 1893; Cajal, 1898] and yet each retina projects to both optic tecta. The pathway taken by nerve impulses from the retina to the ipsilateral tectum is not known. We are at present investigating this problem and therefore do not propose to discuss the possible anatomical pathways. The frog has a binocular visual field with a horizontal extent of about 100. Only the central region of the binocular field (fig. 4, C) is represented through both eyes at one position on the left optic tectum and at another position on the right optic tectum. Only points in the mid-sagittal plane of the animal are represented at symmetrical positions on the two tecta through both eyes. The binocular field to the left of the mid-sagittal line (fig. 4, D) is represented through both eyes on the right tectum only, while the binocular field to the right of the mid-sagittal line (fig. 4, B) is represented through both eyes on the left tectum only. These results suggest a mechanism whereby the frog will strike at a fly only when it is directly in front of its mouth, in the region where the fly will evoke symmetrical patterns of activity through both eyes in both optic tecta. If the fly is in the binocular visual field, but not directly in front of the frog, it will set up activity in one tectum only. The tectum may function as a comparator which obtains the difference between the positions of the retinal image in the two eyes and initiates a strike reaction only when the difference between the evoked pattern on the two optic tecta is zero. All previous conceptions of the mode of projection of the retina to the tectum of submammalian vertebrates are incorrect because they have been based on the belief that the retina projects only to the contralateral tectum.

6 278 Gaze and Jacobson FIG. 3.-The contralateral and ipsilateral projections from the left eye to the rostral half of the right and left optic tecta. Top.-Dorsal view of optic tecta showing electrode positions. Middle.-Chart of visual field of left eye. The frog shows how the perimeter was centred. The perimeter chart covers 1000 outwards from the centre of the field. Bottom.-Tecta showing the representation of the left visual field obtained from the above results. The projection to the right tectum is incomplete in that it only shows half the normal contralateral map. The horizontal meridian (0-180 ) and the vertical meridian ( ) are shown by thick lines on the tectum. The stimulus positions indicated by the symbols * in the visual field project through the left eye to the positions on the right tectum shown by the same symbols. The stimulus positions indicated by O in the visual field project through the left eye to the positions on the left tectum shown by the same symbols. There is a region in the visual field about 600 nasal to the optic axis where stimulus positions for contralateral and ipsilateral projection overlap. Points within this region of field (which represents the animal's mid-sagittal plane) are represented through the left eye on both tecta (compare with fig. 1).

7 Visual Projection in the Frog The present results are also at variance with the theory proposed by Walls 279 [1942, pp. 319 et seq.] that a system of corresponding retinal points does not exist in submammals, but only evolved in mammals together with partial.s,,ri Y1E EY VISUAL F I E LD FIG. 4.-The projection of the various regions of the binocular field on the optic tecta. The perimeter shows the visual field as in fig. 1. The right eye sees field areas A, B, C, D and the left eye sees B, C, D, E. Field area A is seen only by the right eye and projects to the left tectum. Area E is seen only by the left eye and projects to the right tectum. Area B is seen by both eyes and projects through both to the left tectum. Area D is seen by both eyes and projects through both to the right tectum. Area C is seen by both eyes and projects through both to both tecta. The binocular area of field is thus BCD and the binocular, bitectal area of field is C. The connections shown by continuous lines between the eyes and the tecta represent the normal crossed projection via the optic chiasma. The eye-tectal connections indicated by the dotted lines represent the ipsilateral projection from each eye, the paths of which are not known. decussation of the optic nerves and conjugate eye movements. In fact the frog's eyes are fixed in a position of symmetrical divergence, and retraction of the eyes appears to be the only ocular movement. Moreover the frog has a very precise dimensional organization of its visual system, with a system of corresponding retinal points linked with corresponding points on the two tecta. In addition there is a special region in each retina, on the horizontal

8 280 Gaze and Jacobson meridian about 600 temporal to the optic axis, which sends impulses to the same loci on both ipsilateral and contralateral optic tecta. Jacobson [1962] has found that this part of the retina is in the area centralis, with the greatest density of ganglion cells, and that the retino-tectal magnification factor measured along the horizontal meridian of the individual eye is greatest at a point some 600 temporal to the optic axis; that is, at the retinal region corresponding to the binocular point directly in front of the animal. ACKNOWLEDGMENTS Some of the apparatus used in this investigation was provided by a grant from the Royal Society to one of us (R. M. G.). The projection perimeter was provided by the Ross Foundation. REFERENCES CAJAL, S. R. (1898). 'Estructura del kiasma optico", Rev. trim. nticrogr. 3, 15. GAZE, R. M. (1958 a). "The representation of the retina on the optic lobe of the frog", Quart. J. exp. Physiol. 43, 209. GAZE, R. M. (1958 b). "Binocular vision in frogs", J. Physiol. 143, 20P. JACOBSON, M. (1962). "The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count", Quart. J. exp. Physiol. 47, 170. WALLS, G. L. (1942). "The Vertebrate Eye and its Adaptive Radiation". Bull. No. 19, Cranbrook Institute of Science, Michigan. WLASSAK, R. (1893). "Die optischen Leitungsbahnen des Frosches ", Arch. A sat. Physiol., Lpz., Physiol. Abt. Suppl. 1.