CROSSED AND UNCROSSED REPRESENTATION OF THE VISUAL FIELD BY BRISK-SUSTAINED AND BRISK-TRANSIENT CAT RETINAL GANGLION CELLS D. L. KIRK, W. R. LMCK, B. G. CLELANDand
H.
b%SSLE’
Department of Physiology, John Curtin School of Medical Research. Australian National University, Canberra, Australia (Received 16 May 1975)
Abstract-The proiection of the cat’s monocular visual field to the contralateral and ipsilateral @ For both tracts differed for the brisk_sustained and brisk-transient classes of panalion. retinal types all units recorded with receptive field centres more than about @5’ into the temporal visual hemifield had & axons. The transition from crossed coverage of temporal hemifield to m coverage of nasal hemtield was complete at about 0.5’ nasal for the brisk-sustained units but crossed brisk-transient units were found with receptive fields as far nasal as 15.8”. The 50% crossed/fiV/, uncrossed zone for brisk-transient units was located I-2” nasal of that for brisk-sustained units.
INTRODCCTION
optic nerves of mammals undergo a partial decussation at the optic chiasm. In general, fibres from nasal regions of retina cross to the contralateral optic tract while fibres from temporal regions continue to the ipsilateral tract. The uncrossed projection is phylogenetically the more recent and the proportion of uncrossed fibres varies with the degree of frontality of the eyes (Walls, 1942; Polyak. 1957). By virtue of this organisation the nasal and temporal visual fields of each eye are represented respectively in ipsilateral and contralateral optic tracts. However in the cat and to a lesser extent in the monkey (Stone, Leicester and Sherman, 1973) the specificity of this representation is not absolute. Stone (1966) described a pattern of partial decussation in the cat after examination of ganglion cell degeneration in the retinae of animals with unilateral optic tract section. By superimposing density maps of the remaining ganglion cells in both eyes he obtained evidence for a 022mm wide vertical strip, passing through the area centralis in which both crossed and uncrossed cells were present in about equal proportion. He thus provided indirect anatomical evidence that portions of the visual fields of both eyes are projected to both optic tracts. Nasal to the bilaterally represented strip all cells were crossed. Temporal to the strip 75% were uncrossed and 25% were crossed. Physiological evidence for a bilateral projection has been found at higher levels of the cat’s visual pathway. In the lateral geniculate nucleus receptive field centres of cells in layers A and A, extend across the presumed vertical meridian into the ipsilateral hemitield by up to 30’ (Sanderson and Sherman, 1971). In layer B and in the medial interlaminar nucleus The
’ Present address: Fachbereich Psychologie. Universitit Konstanz. D-775 Konstanz, Postfach 733. West Germany.
cells with input from the contralateral eye are found with receptive field centres up to 13’ (Kinston, Vadas and Bishop, 1969) and 36” (Sanderson and Sherman, 1971) into the ipsilateral hemifield. These latter units would presumably receive input from the crossed cells in temporal retina (Stone, 1966). At the cortical level cells have been recorded at the border between areas 17 and 18 (Otsuka and Hassler, 1962) with receptive field centres extending up to about 3-O” into the ipsilateral her&eld (Blakemore, 1969; Joshua and Bishop, 1970; Leicester, 1968; Nikara, Bishop and Pettigrew, 1968). There are indications that interhemispheric connections via the corpus callosum may contribute to the cortical overlap (Berlucchi, Gazzaniga and Rizzolatti, 1967; Berlucchi and Rizzolatti, 1968; Choudhury, Whitteridge and Wilson. 1965; Hubel and Wiesel, 1967). However the overlap described by Leicester survived callosal section and was therefore attributed to the direct geniculo-cortical projection. Knowledge of how the visual field of each eye projects to the optic tracts is a prerequisite to understanding the organisation at higher levels. In recent years it has become apparent that cat retinal ganglion cells form a heterogeneous population of receptive field types (Cleland, Dubin and Levick, 1971; Cleland and Levi& 1974a,b; Enroth-Cugell and Robson, 1966; Fukada, 1971; Stone and Fukuda, 1974a; Stone and Hofhnann, 1972). In view of the likelihood that receptive field differences have functional significance it is important to examine the pattern of part-1 decussation for each receptive field class, the most direct approach being a combination of single uriit recording in the retina and electrical stimulation of the optic tracts. Stone and Fukuda (1974b) independently used this technique, together with recording of retinal field potentials and histological analysis ‘of the retinae of tract sectioned animals to study the decussation pattern of “X-“, “Y-l’ and “W-cells”.
_“6
D. L. KIRK. Lb’ R. LELICF;. B. G. CLELAND and H. Wisst_F In the experiments
to be described
in this
and
maI’s skull b) applcmg a correction to .I braIn ci:la> :cordinate (Reinoso-Suirez. 19611of 9 mm antenor. Shielded bipolar stimulating electrodes I imm bare tips. 1 mm tip separation) were inserted and lowered toward
the
following report 2717 retinal units were examined for type and location of receptive field and for the crossed
or uncrossed destination of their axons. This paper is concerned with the brisk-sustained and brisk-transient units (Cleland and Levick. 1974a). The sluggishconcentric and non-concentric units (Cleland and Levick, 1974a,b) are the subject of the following report. Throughout this and the following paper the term “crossed-uncrossed overlap” will be used in preference to “naso-temporal overlap” (Stone. 1966; Leicester, 1968; Sanderson and Sherman, 1971). The latter implies that a portion of retina or visual field may be at once nasal and temporal. The former refers un-
the optic tracts. Stimulus pulses were Ortec isolator (Model 3656) floating ground. Pulse durations were usually occasionally increased to 1 msec and 100 V were used. lnrra-ocular
ganglion cells having axons passing into the contralateral optic tract will be called “crossed” and those whose axons enter the ipsilateral optic tract will be called “uncrossed”. METHODS
Experiments were performed on 30 adult cats (2Q-4~5 kg). Anaesthesia was induced with 2-4x halothane in a gas mixture (N,O : 0: : CO2 = 70 : 23.4: 13) and maintained during surgical procedures with l-2?: halothane. The vago-sympathetic trunk was severed on the left side to improve ocular stability- (Rod&k, Pettigrew, Bishop and Nikara, 1967) and a tracheal cannula was inserted. Penicillin was given intramuscularly (250,000 units daily).
Procedure
After surgery the animals were artificially respired on the gas mixture (N,O, PI, COJ alone. Muscular paralysis was obtained with contmuous intravenous infusion (gallamine triethiodide 5 m@kg .hr and o-tubocurarine @u)5 mg’kg. hr). Tubocurarine was omitted during inactive stages of the experiment. The recording electrode was first placed centrally on the optic disc and the optic tract stimulating electrodes were lowered into position. The electrical threshold for just detectable stimulus-locked field potentials was monitored as the electrodes were lowered. Satisfactory placement (verified subsequently by brain dissection) was usually indicated
stimulatiorl
The animal’s head was aligned in Horsley-Clarke stereotaxic planes and small craniotomies were made above the right and left optic tracts centred at from 75mm to 9Gnm anterior and 9Qnm lateral. The anterior co-ordinate was determined after examination of an X-ray film of the ani20
1
recordiny
Irma-ocular recordings (Cleland et J[.. 1971) were obtained from ganglion cells and their axons in the left eye with tungsten-in-glass microelectrodes tlevick. 1972) or with 3.5 w NaCl-filled glass micropipettts with tip diameters less than 0.5 pm and impedances at 50 Hz of 12-30 MR. Amplification and display were conventional. The nictitating membrane and ekelids of the left eye were retracted with Neosynephrine eyedrops (E’,) and the left pupil was dilated with atropine drops (I?:). Both right and left comeae were protected with clear plastic contact lenses (zero power). The optic disc and ophthalmoscopically estimated position of the centre of the area centralis were back-projected onto a tangent screen through the sight hole of an ophthalmoscope (Femald and Chase, 1971). An artificial pupil was not routinely used since coverage of a wide area of visual field was desired. Because precise maps of receptive fields were not required. some blurring of the image could be tolerated.
ambiguously to axonal destination independently of position of cell body or receptive field. For brevity,
Electrical
derived from an with respect TV 50 jcsec but uerr amplitudes up ti,
(a)
Crossed
5 ‘5 ;
-2Od
I
I
I
I
I
t
(b)
20
w
Uncrorsed
-20-1 -20
I
I
I
0 Azimuth,
I
20
I
I
Azimuth.
deq
40
deg
Fig. 1. Locations of the receptive field centres of 488 crossed (a) and 745 uncrossed (b) brisk-sustained retinal ganglion cells with the strip of crossed-uncrossed overlap indicated by the shaded area (c). Negative and positive azimuths refer respectively to temporal and nasal visual hernifield of the left eye. Negative and positive elevation to inferior and superior visual field. Azimuth and elevation scales have been magnified ( x 4) in (c).
Axonaf destination of common ganglion cells by thresholds of less than 05 V with 50 psec pulse duration. Initial experiments and to a lesser extent the initial stages of most (26) experiments concentrated on the region of crossed-uncrossed overlap of brisk-sustained receptive fields at the level of the horizontal through the area centralis. Subsequently units were recorded in areas of retina covering the left eye’s visual field from lo” temporal to 40” nasal. Receptive field characteristics were determined with manually controlled contrast targets (Cteland and Levick. 1974a.b) and the geometric centre of each receptive field was marked on the screen. The threshold for electrical stimulation :und the nntidromic conduction latency from the appropriate optic tract were also recorded. Receptive field centre positions on the screen were converted to azimuth and elevation co-ordinates relative to the ophthalmoscopically estimated centre of the area centralis (Bishop. Kozak and Vakkur, 1962). This reference point was adjusted horizontally if necessary to coincide with the centre of the region of crossed-uncrossed overlap of brisk-sustained receptive fields. In the first few experiments it became apparent that crossed and uncrossed brisk-sustained units provided the narrow strip of “nasotemporal overlap” observed anatomically (Stone, 1966). Thev yielded a convenient definition of a presumed vertical meridian (0’ azimuth) to which the crossed-uncrossed distribution of all other unit types could be related. The maximum horizontal adjustment required was 20”. , fal
R
r
loo7
E g
I
1
0
IO
K
50
:
d / -2
I I
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I 20
-
Uncrossed
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Crossed
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i
0 Azimuth,
-2J
j
4
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-4-
03
I
-2
I
i
t
0
1
I
2
-2
I
I
/
0
L
1
2
deg
Fig. 3. Receptive field centre locations of crossed (open circles) and uncrossed (solid circles) brisk-sustained gang lion cells recorded in six individual experiments. Azimuth and elevation conventions are as for Fig. 1.
Crossed N = 488
‘“-,
a
0 i
I
I
4 0
Ati muth,
llncmssed N 8745
-to
2
Fixation of the eye to a metal ring invariably caused some rolling of the eye about its axis. The extent and direction of rolling varied from one experiment to another and it was therefore necessary to apply a torsional correction to each set of data before analysis of the pooled data could b-e undertaken. This was included in the calculations of azimuth and elevation co-ordinates, and involved standardising for all eyes the position angle of the optic disc centre relative to the area centralis and the horizontal meridian (Bishop et al., 1962). This angle has been variously estimated as 24.4” (Bishop et ai.. 1962), 22.2” (Vakkur. Bishop and Kozak, 1963). 20-21’ (Stone. 1966), 16-6’ (Hughes, 1975) and about 16’ (WPssle, Levick and Cleland, 1975). Correction of all optic disc position angles to a standard 22.2” brought the camposite strip of crossed-uncrossed overlap of brisk-sustained receptive fields in line with the vertical. The extent to which this correspondence indicates the true orientation of the optic disc relative to the area centralis and the vertical meridian will be considered in discussion. Preliminary reports of this work have appeared (Kirk. Wlissle. Cleland and Levick. 1974: Kirk. Cleland and Levi&. 1974).
I
2 deg
Fig. 2. (a) Numbers of receptive fields of crossed (open blocks) and uncrossed (solid blocks) brisk-sustained aanalion c&s in a series of‘0.5” wide vertical strips acres’s &e visual field of the left eye. (b) Data of (a) expressed as percentages of crossed (open circles) and of uncrossed (solid circles) units, The two complementary curves have been drawn to illustrate the symmetry of the transition on either side of the line of zero azimuth. The abscissa scale has been magnified (x 5) relative to that of (a).
RESCLTS Brisk-sustained units Recordings were made from 1233 brisk-sustained units of which 488 were crossed and 745 were uncrossed. None could be stimulated from both tracts and IS additionaf units did not respond to stimulation of either tract, presumably because of inadvertent interruption of their axons in the retina during earlier stages of the experiments.
D. L. KIRK. W. R. LEVICK. B. G. CLELA~D and H Wiissr!
‘25
The geometric centrrs of the receptive fields of successfully stimulated units are shown in Fig. I with separate plots for units with crossed (a) and uncrossed (b) axons. In this. and all subsequent figures negative and positive azimuths refer respectively to temporal and nasal visual hemifield. Negative and positive elevations refer respectively to Inferior and superior visual field. ft is evident that, in general. receptive fields of crossed units are confined to the temporal hemifield, those of uncrossed units to the nasal hemifield. However. there is a strip of crossed-uncrossed overlap (represented by the shaded area in Fig. Ic) which varies in width from 06’ to 1,9’ and which passes vertically through the presumed area centralis (00 azimuth. 0’ elevation). Each individual map of receptive fields of all unit types was standard&d to bring this strip in line with the vertical (see Methods). The course of the strip is irregular. This may be a consequence of pooling data from a large number (26) of exFer~ents or of m~hanically induced eye movement caused by vertical adjustment of the electrode tip (see Discussion) as well as a reflection of genuine irregularities, Counts were made of the numbers of receptive fields of crossed and uncrossed units in a series of 05” wide vertical strips across the visual field. The histogram so obtained is shown in Fig. 2a. The trend within the region of crossed-uncrossed overlap is clearer if the data are considered as percentages rather than as absolute numbers of crossed and uncrossed units (Fig. 2b). For this analysis the width of each azimuth bin was O-2”. On opposite sides of the SO?/, point the transition from crossed to uncrossed axons in the temporal to nasal direction is 20
(0)
CfQSSed 1
0
B 5
6 i: 2 2
-20
!” J
I
I
I
I
I
I
(bf
20
”
unciossed
-20 -I -20
I
I
0
I Azimuth.
1
20
I
7
40
dep
Fig. 4. Location of the receptive field centres of 4t4 crossed (a) and 549 uncrossed (b) brisk-transient retinal ganglion cells. Conventions are as for Fig. 1.
Fig. 5. (a) Number of receptive fields of crossed (open blocks) and uncrossed (solid blocks) brisk-transient units in a series of 1.0’ wide vertical strips across the visual field of the left eye. (b) Data of (a) expressed as percentage of crossed units within the range of azimuths indicated by the lengths of the horizontal lines. The vertical bars represent the 9%; confidence limits for each sample percentage.
approximately symmetrical with the transition from uncrossed to crossed in the reverse direction. Individual experiments produced varying amounts of crossed-uncrossed overlap of brisk-sustained receptive fields. Six examples, in which relatively large numbers of units were recorded. are shown in Fig. 3. Widths of overlap range from @48” to t-28”; the maximum (1.28”) was the largest individual vaIue obtained and is less than the maximum width of the pooled overlap strip (Fig. Ic). However, in the latter case. errors inherent in the poofing process, particularly in respect of rotation of each individual map of receptive fields to a standard orientation may have increased the distance between the most nasal crossed and the most temporal uncrossed receptive field. Brisk-transient units Figure 4 shows the geometric centres of the receptive fields of 893 brisk-transient units. 444 were crossed and 449 were uncrossed. None were stimulated from both optic tracts and an additional 9 units could not be stimulated from either tract. Receptive field centres of uncrossed units (b) are confined fo nasal hem%eld and to a limited region (0’ to -0.5’) of temporal hemifteid. Those of crossed units (a) are found throughout the temporal hetni&ld and up to 158” into nasal hetni%ld. The width of the crosseduncrossed overlap region is about 16.5”. The numbers of receptive fields of crossed and uncrossed units in a series of 1’ wide ~~~~aI~~uth strips were counted. The raw data are displayed in histogram form in Fig. Sa and as the percentage of crossed units in Fig. 5b. In the latter graph the lengths
Axonal destination of common ganglion cells
Radius,
Crossed
0
uncrossed
l
/
Temporal
Hemlfjeld
(
Nafol
aey
229
Per cent
0.5
85.7
I .o
04.0
I .5
77.1
Crossed
Hemlfield
Fig. 6. Receptive field centre locations of 71 brisk-transient gan$ion ceils recorded in central retina of one animal, showing the percentage of crossed units within a sena of circles of successively increasing
radius from the centre of the area centralis. of the horizontal lines indicate the azimuth range over which the sample was obtained and the vertical bars show the 95% confidence limits (Diem and Lentner, 1970) for each sample percentage. The percentage of crossed axons was 940/, from - 1’ to 0” and fell sharply to slightly less than 50% at from 1” to 2” nasal. There is a more gradual decrease to about ST/, from 12” to 16” nasal. The transition from crossed to uncrossed axons in the temporal to nasal direction is not symmetrical about the jOo/, point. In one animal an exhaustive recording search was performed in the area centralis. The exhaustiveness of the search was subsequently veriiied by matching the map of brisk-transient receptive fields obtained with the corresponding distribution of alpha cells (Boycott and Wassle. 1974) in a cresyl violet whole mount of the retina. The peak of the alpha cell density was transferred to the map of receptive fields and taken as the centre of the area centralis. Further details of this particular experiment have been described elsewhere (Cleland, Levick and WPssle, 1975). The data give, for this particular retina, the exact percentages of crossed and uncrossed brisk-transient units in the area centralis (Fig. 6). Within a radius of O-5”from the centre the percentage of crossed units was 85.7%. At 1.0” and 1.5” radius it was respectively 84.0 and 77.1%. DISCL’SION
The nature of the projection of the cat’s monocular visual field to the contralateral and ipsilateral optic tracts differed for the brisk-sustained and brisk-transient classes of ganglion cell. For each class an area of crossed-uncrossed overlap was observed. In the case of the brisk-sustained units the maximum horizontal width of this region in a single retina was 1.28”. This may be compared with the 0.9’ wide strip of
naso-temporal overlap described by Stone (1966) but is in closer agreement with the 1.2’ of overlap of crossed and uncrossed “X-cells” reported by Stone and Fukuda (1974b). The composite strip of crossed-uncrossed overlap of brisk-sustained receptive fields obtained by pooling data from 26 experiments was vertical when each visual field map was rotated to a standard optic disc position angle (Bishop er al., 1962) of 22.2’. This was the mean value found by Vakkur et a/. (1963) in anaesthetised, paralysed cats. Hughes (1975) assumed that the visual streak of the cat’s retina would be in line with the horizontal in the conscious animal. Using this anatomical feature as a reference he obtained a mean position angle of 16.63’. He proposed a rotation of the eye (upper margins of the pupils moved medially) by 6” in the anaesthetised, paralysed cat to account for the larger value obtained by Vakkur er a/. (1963). Wassle et al. (1975) reached a similar conclusion. It was assumed in this study that the strip of crossed-uncrossed overlap of brisk-sustained receptive fields should be vertical. This strip has some significance for neurophysiological theories of binocular stereopsis (Bishop, 1973; Bishop and Henry. 1971; Blakemore, 1969) since it is required for neural coding of retinal image disparities for objects in midline vision at depths behind or in front of the fixation point. In order that all points on the midline be represented binocularly in at least one hemisphere it is necessary that the overlap strips for the two eyes be in correspondence. Such a correspondence will be attained only if each strip is vertical. If this argument and that of Hughes (1975) are both correct it is anomalous that rotation to a standard optic disc position angle of 222’ yielded a closer fit to the vertical than rotation to 16.6’. However movements of the record-
ing electrode from the area centralis u here it was initiallr placed for back projection of the retinal landmarks to inferior and superior retina caused rotation of the posterior segment of the eye. The rotations were not checked until the final stages of the study. In one sxpsriment. a movement producing an anttclockwise rotation of the projection of the retina on the tangent screen was found which would have increased the apparent magnitude of the optic disc position angle. Since the angle and position of penetration of the eye by the electrode holder was closely similar in all experiments it is probable that the nature of the distortion and hence the increase in apparent optic disc position angle was similar. The width of crossed-uncrossed overlap of brisktransient receptive fields was about 165’: from 05 temporal to 158” nasal. The transition from crossed to uncrossed axons in the temporal to nasal direction was not symmetrical about the 500,; point. The percentage of crossed axons fell sharply to reach this level at from I ’ to 2’ nasal and then more gradually to zero at beyond 15%‘. A more extensive recording search may have produced units with receptive fields further than 16’ nasal. but if these are present they may be too sparse to be of visual significance. In the vicinity of the presumed vertical meridian (defined as the crossed-uncrossed overlap strip of brisk-sustained receptive fields) the majority of brisktransient units had crossed axons; 254 of 304 (84yd) from 1a temporal to 1’ nasal. Crossed and uncrossed brisk-sustained units with receptive fields in this region were found in approximately equal proportion. Thus each optic tract will receive an asymmetrical representation of this region of visual field from each eye. Contralateral brisk-transient input will predominate over ipsilateral whereas contralateral and ipsilateral brisk-sustained inputs will be equal. Although the pathways carrying information from these two classes of units remain essentially separate through the lateral geniculate nucleus (Cleland er al., 1971; Hoflinann, Stone and Sherman, 1972; Stone and HolTrnann, 1971) inhibitory interactions of brisk-transient on brisk-sustained units have been demonstrated (Singer and Bedworth. 1973). The asymmetry between the crossed and uncrossed brisk-transient pathways representing the vertical meridian suggests that the topographical organisation of these interactions will be complex. The crossed brisk-transient units with receptive fields more than a few degrees nasal are a problem in terms of the eventual destination of their axons. They represent a projection to the central visual centres of the ipsilateral visual field. Such a projection has not been observed in topographical mapping of cortex (Hubel and Wiesel. 1965; Talbot and Marshall, 1941) and has been seen only to a limited extent in the lateral geniculate nucleus (Kinston et nl., 1969; Sanderson, 1971). This will be considered along with a similar problem relating to the sluggish-concentric and non-concentric ganglion cells, in the following paper. Ackno,vledgeme,lrs-D. L. Kirk was supported by a Commonwealth Postgraduate Research Award. H. Wlssle was supported by a Fellowship of the Deutsche Forschungsgemeinschaft. Xliss Erika Beurschgens rendered valuable
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Polyak S. (1957) The Vbtebrate Usual System (Edited by Khiver H.). Univ. of Chicago Press. Reinoso-Suarer F. ( 1961) Topoqraphischer Hirnatlas der Ktrrx. E. Merck AG. Darmstadt. Rodieck R. W., Pettigrew J. D., Bishop P. 0. and Nikara T. (1967) Residual eye movement in receptive field studies of paralysed cats. Msion Res. 7. 107-l IO. Sanderson K. J. (1971) The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J. camp. Nerrrol. 143. 101-108.
131
Sanderson K. J. and Sherman S. M. (1971) i%asotemporal overlap in visual field projected to lateral geniculate nucleus in the cat. J. Seurophysiol. 31. 45M6. Singer W. and Bedworth N. (1973) Inhibitory interaction between X and Y units in the cat lateral geniculate nucleus. Brain Res. 49. 291-307. Stone J. (1966) The nasotemporal division of the cat’s retina. J. camp. Neural. 126. 585-600. Stone J. and Fukuda Y. (1974a) Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Ycells. J. :Veurophysiol. 37. 722-748. Stone J. and Fukuda Y. (1974b) The nasotemporal division of the cat’s retina re-examined in terms of Y-. X- and W-cells. J. camp. Yeurol. 155. 377-394. Stone J. and Hoffmann K.-P. (1971) Conduction velocity as a parameter in the organ&ration of the ahrent relay in the cat’s lateral geniculate nucleus. Brain Res. 32. 4% 459. Stone J. and Hoffmann K.-P. (1972) Very slow-conducting ganglion cells in the cat’s retina: a major new functional type? Brain Res. 43. 610-616. Stone J., Leicester J. and Sherman S. M. (1973) The nasotemporal division of the monkey’s retina. 1. camp. Neurol. ISO. 333-348. Talbot S. A. and Marshall W. H. (1941) Physiological studies on neural mechanisms of visual localisation and discrimination. Am. J. Ophth. 24. 12%1264. Vakkur G. J., Bishop P. 0. and Kozak W. (1963) Visual optics in the cat, including posterior nodal distance and retinal landmarks. tision Res. 3. 289-314. Walls G. L. (1942) The Vertebrate Eye and its Adnptice Radiation. Hafner, New York. Wlssle H., Levick W. R. and Cleland B. G. (1975) The distribution of the alpha type of ganglion cells in the cat’s retina. J. camp. Nectrol. 159. 419-438.
H.
b%SSLE’
Department of Physiology, John Curtin School of Medical Research. Australian National University, Canberra, Australia (Received 16 May 1975)
Abstract-The proiection of the cat’s monocular visual field to the contralateral and ipsilateral @ For both tracts differed for the brisk_sustained and brisk-transient classes of panalion. retinal types all units recorded with receptive field centres more than about @5’ into the temporal visual hemifield had & axons. The transition from crossed coverage of temporal hemifield to m coverage of nasal hemtield was complete at about 0.5’ nasal for the brisk-sustained units but crossed brisk-transient units were found with receptive fields as far nasal as 15.8”. The 50% crossed/fiV/, uncrossed zone for brisk-transient units was located I-2” nasal of that for brisk-sustained units.
INTRODCCTION
optic nerves of mammals undergo a partial decussation at the optic chiasm. In general, fibres from nasal regions of retina cross to the contralateral optic tract while fibres from temporal regions continue to the ipsilateral tract. The uncrossed projection is phylogenetically the more recent and the proportion of uncrossed fibres varies with the degree of frontality of the eyes (Walls, 1942; Polyak. 1957). By virtue of this organisation the nasal and temporal visual fields of each eye are represented respectively in ipsilateral and contralateral optic tracts. However in the cat and to a lesser extent in the monkey (Stone, Leicester and Sherman, 1973) the specificity of this representation is not absolute. Stone (1966) described a pattern of partial decussation in the cat after examination of ganglion cell degeneration in the retinae of animals with unilateral optic tract section. By superimposing density maps of the remaining ganglion cells in both eyes he obtained evidence for a 022mm wide vertical strip, passing through the area centralis in which both crossed and uncrossed cells were present in about equal proportion. He thus provided indirect anatomical evidence that portions of the visual fields of both eyes are projected to both optic tracts. Nasal to the bilaterally represented strip all cells were crossed. Temporal to the strip 75% were uncrossed and 25% were crossed. Physiological evidence for a bilateral projection has been found at higher levels of the cat’s visual pathway. In the lateral geniculate nucleus receptive field centres of cells in layers A and A, extend across the presumed vertical meridian into the ipsilateral hemitield by up to 30’ (Sanderson and Sherman, 1971). In layer B and in the medial interlaminar nucleus The
’ Present address: Fachbereich Psychologie. Universitit Konstanz. D-775 Konstanz, Postfach 733. West Germany.
cells with input from the contralateral eye are found with receptive field centres up to 13’ (Kinston, Vadas and Bishop, 1969) and 36” (Sanderson and Sherman, 1971) into the ipsilateral hemifield. These latter units would presumably receive input from the crossed cells in temporal retina (Stone, 1966). At the cortical level cells have been recorded at the border between areas 17 and 18 (Otsuka and Hassler, 1962) with receptive field centres extending up to about 3-O” into the ipsilateral her&eld (Blakemore, 1969; Joshua and Bishop, 1970; Leicester, 1968; Nikara, Bishop and Pettigrew, 1968). There are indications that interhemispheric connections via the corpus callosum may contribute to the cortical overlap (Berlucchi, Gazzaniga and Rizzolatti, 1967; Berlucchi and Rizzolatti, 1968; Choudhury, Whitteridge and Wilson. 1965; Hubel and Wiesel, 1967). However the overlap described by Leicester survived callosal section and was therefore attributed to the direct geniculo-cortical projection. Knowledge of how the visual field of each eye projects to the optic tracts is a prerequisite to understanding the organisation at higher levels. In recent years it has become apparent that cat retinal ganglion cells form a heterogeneous population of receptive field types (Cleland, Dubin and Levick, 1971; Cleland and Levi& 1974a,b; Enroth-Cugell and Robson, 1966; Fukada, 1971; Stone and Fukuda, 1974a; Stone and Hofhnann, 1972). In view of the likelihood that receptive field differences have functional significance it is important to examine the pattern of part-1 decussation for each receptive field class, the most direct approach being a combination of single uriit recording in the retina and electrical stimulation of the optic tracts. Stone and Fukuda (1974b) independently used this technique, together with recording of retinal field potentials and histological analysis ‘of the retinae of tract sectioned animals to study the decussation pattern of “X-“, “Y-l’ and “W-cells”.
_“6
D. L. KIRK. Lb’ R. LELICF;. B. G. CLELAND and H. Wisst_F In the experiments
to be described
in this
and
maI’s skull b) applcmg a correction to .I braIn ci:la> :cordinate (Reinoso-Suirez. 19611of 9 mm antenor. Shielded bipolar stimulating electrodes I imm bare tips. 1 mm tip separation) were inserted and lowered toward
the
following report 2717 retinal units were examined for type and location of receptive field and for the crossed
or uncrossed destination of their axons. This paper is concerned with the brisk-sustained and brisk-transient units (Cleland and Levick. 1974a). The sluggishconcentric and non-concentric units (Cleland and Levick, 1974a,b) are the subject of the following report. Throughout this and the following paper the term “crossed-uncrossed overlap” will be used in preference to “naso-temporal overlap” (Stone. 1966; Leicester, 1968; Sanderson and Sherman, 1971). The latter implies that a portion of retina or visual field may be at once nasal and temporal. The former refers un-
the optic tracts. Stimulus pulses were Ortec isolator (Model 3656) floating ground. Pulse durations were usually occasionally increased to 1 msec and 100 V were used. lnrra-ocular
ganglion cells having axons passing into the contralateral optic tract will be called “crossed” and those whose axons enter the ipsilateral optic tract will be called “uncrossed”. METHODS
Experiments were performed on 30 adult cats (2Q-4~5 kg). Anaesthesia was induced with 2-4x halothane in a gas mixture (N,O : 0: : CO2 = 70 : 23.4: 13) and maintained during surgical procedures with l-2?: halothane. The vago-sympathetic trunk was severed on the left side to improve ocular stability- (Rod&k, Pettigrew, Bishop and Nikara, 1967) and a tracheal cannula was inserted. Penicillin was given intramuscularly (250,000 units daily).
Procedure
After surgery the animals were artificially respired on the gas mixture (N,O, PI, COJ alone. Muscular paralysis was obtained with contmuous intravenous infusion (gallamine triethiodide 5 m@kg .hr and o-tubocurarine @u)5 mg’kg. hr). Tubocurarine was omitted during inactive stages of the experiment. The recording electrode was first placed centrally on the optic disc and the optic tract stimulating electrodes were lowered into position. The electrical threshold for just detectable stimulus-locked field potentials was monitored as the electrodes were lowered. Satisfactory placement (verified subsequently by brain dissection) was usually indicated
stimulatiorl
The animal’s head was aligned in Horsley-Clarke stereotaxic planes and small craniotomies were made above the right and left optic tracts centred at from 75mm to 9Gnm anterior and 9Qnm lateral. The anterior co-ordinate was determined after examination of an X-ray film of the ani20
1
recordiny
Irma-ocular recordings (Cleland et J[.. 1971) were obtained from ganglion cells and their axons in the left eye with tungsten-in-glass microelectrodes tlevick. 1972) or with 3.5 w NaCl-filled glass micropipettts with tip diameters less than 0.5 pm and impedances at 50 Hz of 12-30 MR. Amplification and display were conventional. The nictitating membrane and ekelids of the left eye were retracted with Neosynephrine eyedrops (E’,) and the left pupil was dilated with atropine drops (I?:). Both right and left comeae were protected with clear plastic contact lenses (zero power). The optic disc and ophthalmoscopically estimated position of the centre of the area centralis were back-projected onto a tangent screen through the sight hole of an ophthalmoscope (Femald and Chase, 1971). An artificial pupil was not routinely used since coverage of a wide area of visual field was desired. Because precise maps of receptive fields were not required. some blurring of the image could be tolerated.
ambiguously to axonal destination independently of position of cell body or receptive field. For brevity,
Electrical
derived from an with respect TV 50 jcsec but uerr amplitudes up ti,
(a)
Crossed
5 ‘5 ;
-2Od
I
I
I
I
I
t
(b)
20
w
Uncrorsed
-20-1 -20
I
I
I
0 Azimuth,
I
20
I
I
Azimuth.
deq
40
deg
Fig. 1. Locations of the receptive field centres of 488 crossed (a) and 745 uncrossed (b) brisk-sustained retinal ganglion cells with the strip of crossed-uncrossed overlap indicated by the shaded area (c). Negative and positive azimuths refer respectively to temporal and nasal visual hernifield of the left eye. Negative and positive elevation to inferior and superior visual field. Azimuth and elevation scales have been magnified ( x 4) in (c).
Axonaf destination of common ganglion cells by thresholds of less than 05 V with 50 psec pulse duration. Initial experiments and to a lesser extent the initial stages of most (26) experiments concentrated on the region of crossed-uncrossed overlap of brisk-sustained receptive fields at the level of the horizontal through the area centralis. Subsequently units were recorded in areas of retina covering the left eye’s visual field from lo” temporal to 40” nasal. Receptive field characteristics were determined with manually controlled contrast targets (Cteland and Levick. 1974a.b) and the geometric centre of each receptive field was marked on the screen. The threshold for electrical stimulation :und the nntidromic conduction latency from the appropriate optic tract were also recorded. Receptive field centre positions on the screen were converted to azimuth and elevation co-ordinates relative to the ophthalmoscopically estimated centre of the area centralis (Bishop. Kozak and Vakkur, 1962). This reference point was adjusted horizontally if necessary to coincide with the centre of the region of crossed-uncrossed overlap of brisk-sustained receptive fields. In the first few experiments it became apparent that crossed and uncrossed brisk-sustained units provided the narrow strip of “nasotemporal overlap” observed anatomically (Stone, 1966). Thev yielded a convenient definition of a presumed vertical meridian (0’ azimuth) to which the crossed-uncrossed distribution of all other unit types could be related. The maximum horizontal adjustment required was 20”. , fal
R
r
loo7
E g
I
1
0
IO
K
50
:
d / -2
I I
I
I 20
-
Uncrossed
..-..--
Crossed
“a, \
i
0 Azimuth,
-2J
j
4
g I -G B I5
2-
o-2-
-4-
03
I
-2
I
i
t
0
1
I
2
-2
I
I
/
0
L
1
2
deg
Fig. 3. Receptive field centre locations of crossed (open circles) and uncrossed (solid circles) brisk-sustained gang lion cells recorded in six individual experiments. Azimuth and elevation conventions are as for Fig. 1.
Crossed N = 488
‘“-,
a
0 i
I
I
4 0
Ati muth,
llncmssed N 8745
-to
2
Fixation of the eye to a metal ring invariably caused some rolling of the eye about its axis. The extent and direction of rolling varied from one experiment to another and it was therefore necessary to apply a torsional correction to each set of data before analysis of the pooled data could b-e undertaken. This was included in the calculations of azimuth and elevation co-ordinates, and involved standardising for all eyes the position angle of the optic disc centre relative to the area centralis and the horizontal meridian (Bishop et al., 1962). This angle has been variously estimated as 24.4” (Bishop et ai.. 1962), 22.2” (Vakkur. Bishop and Kozak, 1963). 20-21’ (Stone. 1966), 16-6’ (Hughes, 1975) and about 16’ (WPssle, Levick and Cleland, 1975). Correction of all optic disc position angles to a standard 22.2” brought the camposite strip of crossed-uncrossed overlap of brisk-sustained receptive fields in line with the vertical. The extent to which this correspondence indicates the true orientation of the optic disc relative to the area centralis and the vertical meridian will be considered in discussion. Preliminary reports of this work have appeared (Kirk. Wlissle. Cleland and Levick. 1974: Kirk. Cleland and Levi&. 1974).
I
2 deg
Fig. 2. (a) Numbers of receptive fields of crossed (open blocks) and uncrossed (solid blocks) brisk-sustained aanalion c&s in a series of‘0.5” wide vertical strips acres’s &e visual field of the left eye. (b) Data of (a) expressed as percentages of crossed (open circles) and of uncrossed (solid circles) units, The two complementary curves have been drawn to illustrate the symmetry of the transition on either side of the line of zero azimuth. The abscissa scale has been magnified (x 5) relative to that of (a).
RESCLTS Brisk-sustained units Recordings were made from 1233 brisk-sustained units of which 488 were crossed and 745 were uncrossed. None could be stimulated from both tracts and IS additionaf units did not respond to stimulation of either tract, presumably because of inadvertent interruption of their axons in the retina during earlier stages of the experiments.
D. L. KIRK. W. R. LEVICK. B. G. CLELA~D and H Wiissr!
‘25
The geometric centrrs of the receptive fields of successfully stimulated units are shown in Fig. I with separate plots for units with crossed (a) and uncrossed (b) axons. In this. and all subsequent figures negative and positive azimuths refer respectively to temporal and nasal visual hemifield. Negative and positive elevations refer respectively to Inferior and superior visual field. ft is evident that, in general. receptive fields of crossed units are confined to the temporal hemifield, those of uncrossed units to the nasal hemifield. However. there is a strip of crossed-uncrossed overlap (represented by the shaded area in Fig. Ic) which varies in width from 06’ to 1,9’ and which passes vertically through the presumed area centralis (00 azimuth. 0’ elevation). Each individual map of receptive fields of all unit types was standard&d to bring this strip in line with the vertical (see Methods). The course of the strip is irregular. This may be a consequence of pooling data from a large number (26) of exFer~ents or of m~hanically induced eye movement caused by vertical adjustment of the electrode tip (see Discussion) as well as a reflection of genuine irregularities, Counts were made of the numbers of receptive fields of crossed and uncrossed units in a series of 05” wide vertical strips across the visual field. The histogram so obtained is shown in Fig. 2a. The trend within the region of crossed-uncrossed overlap is clearer if the data are considered as percentages rather than as absolute numbers of crossed and uncrossed units (Fig. 2b). For this analysis the width of each azimuth bin was O-2”. On opposite sides of the SO?/, point the transition from crossed to uncrossed axons in the temporal to nasal direction is 20
(0)
CfQSSed 1
0
B 5
6 i: 2 2
-20
!” J
I
I
I
I
I
I
(bf
20
”
unciossed
-20 -I -20
I
I
0
I Azimuth.
1
20
I
7
40
dep
Fig. 4. Location of the receptive field centres of 4t4 crossed (a) and 549 uncrossed (b) brisk-transient retinal ganglion cells. Conventions are as for Fig. 1.
Fig. 5. (a) Number of receptive fields of crossed (open blocks) and uncrossed (solid blocks) brisk-transient units in a series of 1.0’ wide vertical strips across the visual field of the left eye. (b) Data of (a) expressed as percentage of crossed units within the range of azimuths indicated by the lengths of the horizontal lines. The vertical bars represent the 9%; confidence limits for each sample percentage.
approximately symmetrical with the transition from uncrossed to crossed in the reverse direction. Individual experiments produced varying amounts of crossed-uncrossed overlap of brisk-sustained receptive fields. Six examples, in which relatively large numbers of units were recorded. are shown in Fig. 3. Widths of overlap range from @48” to t-28”; the maximum (1.28”) was the largest individual vaIue obtained and is less than the maximum width of the pooled overlap strip (Fig. Ic). However, in the latter case. errors inherent in the poofing process, particularly in respect of rotation of each individual map of receptive fields to a standard orientation may have increased the distance between the most nasal crossed and the most temporal uncrossed receptive field. Brisk-transient units Figure 4 shows the geometric centres of the receptive fields of 893 brisk-transient units. 444 were crossed and 449 were uncrossed. None were stimulated from both optic tracts and an additional 9 units could not be stimulated from either tract. Receptive field centres of uncrossed units (b) are confined fo nasal hem%eld and to a limited region (0’ to -0.5’) of temporal hemifteid. Those of crossed units (a) are found throughout the temporal hetni&ld and up to 158” into nasal hetni%ld. The width of the crosseduncrossed overlap region is about 16.5”. The numbers of receptive fields of crossed and uncrossed units in a series of 1’ wide ~~~~aI~~uth strips were counted. The raw data are displayed in histogram form in Fig. Sa and as the percentage of crossed units in Fig. 5b. In the latter graph the lengths
Axonal destination of common ganglion cells
Radius,
Crossed
0
uncrossed
l
/
Temporal
Hemlfjeld
(
Nafol
aey
229
Per cent
0.5
85.7
I .o
04.0
I .5
77.1
Crossed
Hemlfield
Fig. 6. Receptive field centre locations of 71 brisk-transient gan$ion ceils recorded in central retina of one animal, showing the percentage of crossed units within a sena of circles of successively increasing
radius from the centre of the area centralis. of the horizontal lines indicate the azimuth range over which the sample was obtained and the vertical bars show the 95% confidence limits (Diem and Lentner, 1970) for each sample percentage. The percentage of crossed axons was 940/, from - 1’ to 0” and fell sharply to slightly less than 50% at from 1” to 2” nasal. There is a more gradual decrease to about ST/, from 12” to 16” nasal. The transition from crossed to uncrossed axons in the temporal to nasal direction is not symmetrical about the jOo/, point. In one animal an exhaustive recording search was performed in the area centralis. The exhaustiveness of the search was subsequently veriiied by matching the map of brisk-transient receptive fields obtained with the corresponding distribution of alpha cells (Boycott and Wassle. 1974) in a cresyl violet whole mount of the retina. The peak of the alpha cell density was transferred to the map of receptive fields and taken as the centre of the area centralis. Further details of this particular experiment have been described elsewhere (Cleland, Levick and WPssle, 1975). The data give, for this particular retina, the exact percentages of crossed and uncrossed brisk-transient units in the area centralis (Fig. 6). Within a radius of O-5”from the centre the percentage of crossed units was 85.7%. At 1.0” and 1.5” radius it was respectively 84.0 and 77.1%. DISCL’SION
The nature of the projection of the cat’s monocular visual field to the contralateral and ipsilateral optic tracts differed for the brisk-sustained and brisk-transient classes of ganglion cell. For each class an area of crossed-uncrossed overlap was observed. In the case of the brisk-sustained units the maximum horizontal width of this region in a single retina was 1.28”. This may be compared with the 0.9’ wide strip of
naso-temporal overlap described by Stone (1966) but is in closer agreement with the 1.2’ of overlap of crossed and uncrossed “X-cells” reported by Stone and Fukuda (1974b). The composite strip of crossed-uncrossed overlap of brisk-sustained receptive fields obtained by pooling data from 26 experiments was vertical when each visual field map was rotated to a standard optic disc position angle (Bishop er al., 1962) of 22.2’. This was the mean value found by Vakkur et a/. (1963) in anaesthetised, paralysed cats. Hughes (1975) assumed that the visual streak of the cat’s retina would be in line with the horizontal in the conscious animal. Using this anatomical feature as a reference he obtained a mean position angle of 16.63’. He proposed a rotation of the eye (upper margins of the pupils moved medially) by 6” in the anaesthetised, paralysed cat to account for the larger value obtained by Vakkur er a/. (1963). Wassle et al. (1975) reached a similar conclusion. It was assumed in this study that the strip of crossed-uncrossed overlap of brisk-sustained receptive fields should be vertical. This strip has some significance for neurophysiological theories of binocular stereopsis (Bishop, 1973; Bishop and Henry. 1971; Blakemore, 1969) since it is required for neural coding of retinal image disparities for objects in midline vision at depths behind or in front of the fixation point. In order that all points on the midline be represented binocularly in at least one hemisphere it is necessary that the overlap strips for the two eyes be in correspondence. Such a correspondence will be attained only if each strip is vertical. If this argument and that of Hughes (1975) are both correct it is anomalous that rotation to a standard optic disc position angle of 222’ yielded a closer fit to the vertical than rotation to 16.6’. However movements of the record-
ing electrode from the area centralis u here it was initiallr placed for back projection of the retinal landmarks to inferior and superior retina caused rotation of the posterior segment of the eye. The rotations were not checked until the final stages of the study. In one sxpsriment. a movement producing an anttclockwise rotation of the projection of the retina on the tangent screen was found which would have increased the apparent magnitude of the optic disc position angle. Since the angle and position of penetration of the eye by the electrode holder was closely similar in all experiments it is probable that the nature of the distortion and hence the increase in apparent optic disc position angle was similar. The width of crossed-uncrossed overlap of brisktransient receptive fields was about 165’: from 05 temporal to 158” nasal. The transition from crossed to uncrossed axons in the temporal to nasal direction was not symmetrical about the 500,; point. The percentage of crossed axons fell sharply to reach this level at from I ’ to 2’ nasal and then more gradually to zero at beyond 15%‘. A more extensive recording search may have produced units with receptive fields further than 16’ nasal. but if these are present they may be too sparse to be of visual significance. In the vicinity of the presumed vertical meridian (defined as the crossed-uncrossed overlap strip of brisk-sustained receptive fields) the majority of brisktransient units had crossed axons; 254 of 304 (84yd) from 1a temporal to 1’ nasal. Crossed and uncrossed brisk-sustained units with receptive fields in this region were found in approximately equal proportion. Thus each optic tract will receive an asymmetrical representation of this region of visual field from each eye. Contralateral brisk-transient input will predominate over ipsilateral whereas contralateral and ipsilateral brisk-sustained inputs will be equal. Although the pathways carrying information from these two classes of units remain essentially separate through the lateral geniculate nucleus (Cleland er al., 1971; Hoflinann, Stone and Sherman, 1972; Stone and HolTrnann, 1971) inhibitory interactions of brisk-transient on brisk-sustained units have been demonstrated (Singer and Bedworth. 1973). The asymmetry between the crossed and uncrossed brisk-transient pathways representing the vertical meridian suggests that the topographical organisation of these interactions will be complex. The crossed brisk-transient units with receptive fields more than a few degrees nasal are a problem in terms of the eventual destination of their axons. They represent a projection to the central visual centres of the ipsilateral visual field. Such a projection has not been observed in topographical mapping of cortex (Hubel and Wiesel. 1965; Talbot and Marshall, 1941) and has been seen only to a limited extent in the lateral geniculate nucleus (Kinston et nl., 1969; Sanderson, 1971). This will be considered along with a similar problem relating to the sluggish-concentric and non-concentric ganglion cells, in the following paper. Ackno,vledgeme,lrs-D. L. Kirk was supported by a Commonwealth Postgraduate Research Award. H. Wlssle was supported by a Fellowship of the Deutsche Forschungsgemeinschaft. Xliss Erika Beurschgens rendered valuable
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Cleland B. G. and Levick W. R. (1974a) Brisk and sluggish concentrically organized ganglion cells in the Cat’s retina. J. Physiol.,
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