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The projection of the visual field upon the retina of the pigeon
Vi&n Res. Vol. 27, No. I, pp. 31-40. 1987 printed in Great Britain.All rights ~~twd
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THE PROJECTION OF THE VISUAL FIELD THE RETINA OF THE PIGEON
0042-6989/87 $3.00 + 0.00 1987 PergamonJournalsLtd
UPON
B. P. HAYES, W. Horns, A. L. HOLDENand J. C. Low The Department of Visual Science, Institute of Ophthalmology, Judd St., London WC1 H9QS. England (Received 2 January 1986; in revised form 1 April 1986)
Abstract-Co-ordinates in the visual field of the pigeon eye were located in the eye cup anatomically by marking the position of the trans-scleral image. The retina1horizon and vertical meridia at azimuths 0 deg (frontal field) and 90 deg (lateral field) were located. Approximately 18 deg of binocular field are available in frontal vision and the frontal meridian projects to temporal retina outside the red field. Spatial distributions of ganglion cells, displaced ganglion cells, and centrifugal terminals were located in the eye cup. Retina1 magnification factors in the posterior pole and temporal periphery are close to 120 pm/deg. Pigeon
Visual field
Retina
Binocular vision
INTRODUCI’ION
There have been many studies of the morphology, quantitative histology and physiology of the pigeon retina (Humphrey, 1961; Meyer, 1977; Hayes, 1982; Holden 1982), of the pigeon’s visual behaviour and visual field (Rochon-Duvigneaud, 1943; Hodos et al., 1985; Martin and Young, 1983) and of the representation of the retina in the central visual pathways (Hamdi and Whitteridge, 1954; Clarke and Whitteridge, 1976). Yet little is known of the optical design of this panoramic eye, and of the design differences between a panoramic and a foveocentric optical organisation. There have been few attempts to link the spatal distribution of retinal cell types to the way the eye is aligned in, and provides a view of, the visual field. Such an analysis could provide insight into the marked regional specialisations of the pigeon retina. This paper begins such a study by relating co-ordinates of the visual field to their retinal projections, thus permitting a description of the field of view of topographical features such as the “red-field” of the retina, of the field coordinates of the pecten, and of the displaced ganglion cells and centrifugal terminals (Hayes and Holden, 1983a, 1983b). The observations are made post-mortem, using the technique of Rochon-Duvigneaud (1922) of observing the trans-scleral image of a light source. In addition to marking the co-ordinates of the visual field, our experiments provide measurements of reti-
Cell distribution
Magnification factor
nal magnification factors both in the central and the peripheral visual field. These are of some interest since it has been calculated for the human eye that there is a marked reduction in magnification in the retinal periphery (Sine, 1934; Drasdo and Flower, 1974; Fitzke, 1986) and it is natural to enquire whether this feature is found in an eye with a panoramic visual field.
METHODS
The observations were made on 10 feral pigeons, Columba livia. The animals were sacrificed under ether anaesthesia. The head was held in a stereotactic system with ear bars, and a beak bar that could be adjusted so that the beak tip was 35 deg down from the interpupillary line. A bright 20 W quartz-halogen lamp with 2mm filament (Thorn, M-20) was positioned 50 cm from the eye in a perimeter system. The bulb could be rotated about the centre of the pupil in a vertical arc through varying elevations in the visual field. Angles below the horizontal were designated as negative elevations, and above the horizontal as positive elevations. The head could be rotated about the centre of the pupil on a milling machine stand, which was equivalent to the light source being displaced in a horizontal arc through varying angles of azimuth. Azimuth Odeg in the visual field was defined as frontal, parallel to the saggital plane of the head. These perimeter motions define a 31
B. P. HAYESet al.
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simple co-ordinate system for the visual field of each eye, directly analogous to the cartographical coordinates of the earth; lines of iso-elevation are equivalent to the lines of latitude, and lines of constant azimuth (vertical meridia) are equivalent to the lines of longitude. A visual pole occurs at the upper and lower visual field, where the meridia meet. The geographical equator is equivalent to the visual horizon. A diagrammatic view of the visual field co-ordinates is given in Fig. l(a). The head was dissected to expose a limited region of the sclera of the left eye, centred either at the fundal pole, or at the temporal periphery of the globe, for locating central field coordinates (in the region of visual field coordinates azimuth 90deg and elevation Odeg) and peripheral field coordinates (azimuth 0 deg, elevation 0 to - 70 deg), respectively. The position of the light source was adjusted, and its coordinates were noted. The trans-scleral image of the light source (Rochon-Duvigneaud, 1922) was observed under a dissecting microscope, and a cautery bum was applied to the sclera over the image, in order to mark the position of the image in the retina, through the outer coats of the eye. Three to fourteen burns were made in each eye. The lamp was usually displaced with 10deg intervals between adjacent positions, so that retinal marks were separated by approx. 1 mm. The scleral image was less easy to locate at the retinal periphery, because of the reduction in intensity due to the shape of the pupil in the periphery of the visual field.
The eye was excised and fixed in phosphate buffered 3% glutaraldehyde, as described in Hayes et al. (1987). The anterior segment and vitreous were removed and the burns were located in the eye cup. The eye cup was photographed at x 1.44 magnification. The distances between the centres of the burns were measured from prints at x 7.2 magnification, as described below. In order to facilitate comparison of the macrophotographs of eye cups, a standard perspective view was computed of the visual field co-ordinates transferred to a hemisphere 6.8 mm in radius, and imaged in the film plane of the macro-camera. The value of 6.8 mm as the radius for a standard eye cup was arrived at after curve fitting of retinal outlines with a mainframe computer (Euclid System, University College, London). Retinal outlines (at the plane of the photoreceptors) were traced from macro-photographs of hemisected eye-cups, using a bit pad for data entry. It was found that sections of the retina could be well fitted by segments of a circle, and the value of 6.8 mm was derived from three computer fitted experiments. The computation of the perspective view was carried out in a laboratory microcomputer, and plots were produced on a Hewlett-Packard 7470A plotter. The accuracy of the computer model, and the scale distortions introduced by photograph of a hemispherical cup were checked by photography of a cup containing equidistant calibration marks. Linear distance on the photograph was near-proportional to
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go,-90 D
T
.‘j i
go,-90
visual
field
go,90 v
eye
cup
Fig. 1. Diagrammatic representation of the visual field co-ordinates (a) and eye cup co-ordinates (b) used in this study. The number pairs give azimuth and elevation values, and the letters give anatomical locations in the eye cup; N, nasal; T, temporal; D, dorsal; V, ventral. The oblique outline in the temporal to ventral quadrant represents the pecten base.
Pigeon visual field
degrees of arc angle for eccentricities up t0 40 deg from the geometric centre of the cup; and the computed values agreed closely with the measured distances. It should be noted that eye cup co-ordinates are displaced from the visual field co-ordinates. They would correspond exactly only if visual field co-ordinate elevation 0 deg, azimuth 90 deg projected exactly to the geometrical centre of the eye cup. A diagrammatic view of the eye cup co-ordinates is given in Fig. l(b). The positions of retinal marks and the pecten, area centralis and outline of the red field were drawn onto computer plots of the standard perspective view of the eye cup by projecting macrophotographs in an enlarger. The enlarger magnification was varied to match the rim of the eye cup with the outline of the computer plot and the orientation adjusted to bring the pecten to an angle of 72 deg to the horizontal, which is the pecten angle in the alert, unrestrained, pigeon, (Hayes and Holden, 1983a) and the pecten angle observed when the bill is held 35 deg down in the stereotactic instrument. Retinal magnification factors @m of retinal distance/degree arc in the visual field) were calculated. Distance between the centres of retinal marks was measured on the eye-cup photographs. Retinal distances were measured near the geometrical centre of the whole eye cup as straight-line distances on the photograph. Where marks were close to the edge of the eye-cup, the cup was bisected so that its oral edge could be rotated to be viewed axially at the centre of the photograph, where the representation of the curved surface most closely approximated to Retinal planar geometry. magnification factors were calculated as the ratio of retinal arc length to the angle subtended in the visual field (pm per degree). Arc length in the visual field was computed from the visual field co-ordinates noted during the experiment as: arc = cos-’ [(sin a* sin b)
where the symbol * indicates multiplication, a and b are the elevations associated with two readings, and P is their difference in azumuth. Retinal arc length was computed assuming that the retinal surface is spherical, and of radius 6.8 mm. In order to compare cell and fibre distributions in the retina with visual field co-ordinates
projection
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a single retinal map incorporating isodensity lines of ganglion cell, displaced ganglion cell and centrifugal terminal distributions and retinal landmarks was made from the data of Hayes and Holden (1983a, b). The map of the flat-mount was reconstructed into a cup shape by taping together the edges that represent the cuts made before the retina was flattened. The reconstruction was then photographed with the macrocamera. The negative was projected to fill a computer plotted perspective view of the eye cup and the pecten angle adjusted to 72 deg. The isodensity lines and retinal landmarks were then transferred to the perspective view of the eye cup. RESULTS
(1) The appearance of the retinal marks Electrocautery produced pits of approx. 0.7mm diameter in the external surface of the sclera. On examination of the eye cup the macroscopic appearance of the fundus was well preserved and the pecten, red field and sometimes the pit of the area centralis could be seen (Fig. 2). Seventy-seven percent of the bums produced a mark on the retina, clearly discemible in the eye cup (Figs 2 and 3). The majority of retinal marks consisted of a nearly circular central white area of mean diameter 0.8 f 0.3 mm (n = 50) surrounded by a narrow grey halo of 0.2 &-0.04 mm (n = 28) mean width. Occasionally only a grey mark of 0.5 to 0.8 mm diameter was seen. When a scleral burn did not produce a mark on the retina a fine insect pin (0.15 mm diameter) was inserted perpendicular to the sclera, through the centre of the scleral pit. This produced a fine tear in the retina extending for about 0.5 mm. The centres of retinal marks were taken as the intersection of two diameters mutually at right angles. Posterior retina marks (of which 49 were recovered) were distributed in a nearly square grid over the central 10% of the retinal area (Fig. 2). Temporal retinal marks (Fig. 3) (46 were recovered) were not so evenly distributed; they were in a nearly square grid near the horizontal meridian but they showed horizontal convergence at decreasing elevation in the visual field. (2) The location of the horizon and vertical meridia Retinal marks were plotted onto computer generated perspective views of the eye cup (e.g.
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B. P. H Am
Fig. 4). Horizon marks (visual field elevation 0 deg) were found to lie approximately parallel to the horizontal grid lines at eye cup corordinates + 5 deg elevation. Marks at azimuth 90 deg in the visual field were nearly parallel to the vertical grid lines at eye cup co-ordinates azimuth 105 deg. This azimuth 90 deg, elevation Odeg, in the visual field i.e. lateral to the head and at the level of the pupil, projected approx. 15 deg nasal and 5 deg ventral to the centre of the eye cup (Fig. 4). This was about 17 deg nasal to the position of the area centralis. As can be seen in Fig. 4, marks made at azimuth 0 deg in the visual field were found parallel to the temporal edge of the eye cup, at about 15 deg from the rim (Fig. 4) (cup coordinates azimuth 15 deg) and just outside the temporal edge of the red field. The red field was an elliptical area in the dorsal third of the eye cup (Fig. 4) and a single mark made at visual field co-ordinates azimuth 85 deg, elevation - 60 deg was located near its centre. The head of the pecten was found to be located at 20 deg temporal and 10 deg ventral to the centre of the eye cup (Fig. 4).
et al.
(3) The margins and extent of the visual field Marks made at azimuth Odeg in the visual field, i.e. with the lamp positioned directly in front of the head, were found to lie within 10-20 deg of the rim of the eye cup (Fig. 4). A narrow band of temporal retina is therefore available for binocular overlap of the frontal visual field. The width of this binocular region, measured from the ora serrata, varied between 1.3 mm at -30 deg elevation and 0.55 mm at - 70 deg elevation (Fig. 3). (4) Retinal ~agn~~~tio~ in the v~~a~~eld Measurements of retinal magnification factors are summarised in the histograms shown in Fig. 5. Measurements taken at the posterior pole of the eye are shown in Fig. 5(a), based on 203 readings, and measurements taken in the temporal periphery (in the region of azimuth 0 deg in the visual field) are shown in Fig. 5(b), based on 164 readings. The mean retinal magnification at the posterior pole was 119.27 pm, standard deviation 12.38 pm: at the retinal periphery the mean temporal 0
Fig. 4. Perspective view of the eye cup (grid lines are 10 deg apart) showing marks of the vertical mcridia, horizon and retinal features, The outline of the red field (r) is shown dotted. Solid circles: azimuth 90 deg marks; solid squares: elevation Odeg marks; solid triangles: azimuth Odeg marks; open circle: md field mark at azimuth 85, elevation -60. The approximate projections of the vertical meridian at visual fieId azimuth 90 deg and of the horizon (visual field elevation 0 deg) are shown by dotted tines. D, dorsal; Y, ventral; N, nasat; T, temporal; p, pecten; y, yellow field.
Fig. 2. Macro-photograph of an eye cup showing marks on the retina which resulted from 10 scleral bums spaced 10deg apart, near the centre of the visual field (azimuth 70-100, elevation IO to -2Odeg). The centres of the marks from which measurements were taken are shown (dots). Numbers indicate the visual field co-ordinates of the light source. A retinal detachment (d) in the naso-temporal periphery occurred during dissection. The red field (r, outline dotted) appears paler than the yellow field (y). D, dorsal; V, ventral; N, nasal; T, temporal; p, pecten. Scale line: 1 mm.
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Fig. 3. Macro-photograph of the temporal half of an eye cup from an eye which received 13 scleral bums in the temporal peripheral retina spaced lOdeg apart in visual space (azimuth C-30, elevation -20 to - 70 deg). Numbers indicate the visual co-ordinates of the light source. The cup has been tilted to bring the marks close to the camera axis for measurement of distances on the retina (dots show the centres of the marks). The diameter of the marks is 0.5-l .4 mm. D, dorsal; V, ventral; r, red field (outline dotted); p, pecten; n, optic nerve; 0, ora serrata. Scale line: I mm.
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Pigeon visual field projection 50
r
(a)
(b)
r Fig. 5. Histograms of retinal magnification factors. Abscissa, magnification factor, (Ctm/deg); ordinate, percentage frequency. Histogram (a) derived from measurements at the posterior pole of the eye; histogram (h) derived from measurements at the temporal periphery.
magnification was 119.47 pm, standard deviation 16.62pm. These means are not significantly different using Student’s r-test: (given the sample sizes and variances, a difference in mean of f 1.5 pm would be statistically significant at the 0.05 level). The two distributions are not significantly different using the Mann-Whitney U-test. Thus retinal magnification is essentially identical in the central and the peripheral visual field of the pigeon eye. (5) Reconstruction of cell and terminal distributions in the retina The distribution maps of ganglion cells, displaced ganglion cells and centrifugal terminals
were reconstructed onto a perspective view of the eye cup, and are illustrated in Fig. 6. Bands of high density of displaced ganglion cells and centrifugal terminals were found near the horizontal meridian of the eye cup, and the visual horizon, and they were oriented at approx. 15 deg to the horizontal grid. These bands extended from the posterior pole to the mid temporal region of the eye cup. Within the bands of high density concentrations of ganglion cells, displaced ganglion cells and centrifugal terminals were found near the centre of the cup at cup co-ordinates azimuth 85-95 deg, elevation 0-10deg. This area of the cup views the visual field close to the horizon, near visual field azimuth 75 deg. Concentrations of displaced ganglion cells and centrifugal terminals also occur in the mid temporal retina near the horizon, and these view the frontal visual field just below the horizon at azimuth 30-40 deg, elevation -5 to - 10 deg. High densities of ganglion cells are found near the centre of the eye cup, with a peak density adjacent to the fovea. Figure 6 also includes a reconstructed outline of the red field, which matches that found by macro-photography. Towards the centre of the red field a concentration of ganglion cells is found at visual field co-ordinates azimuth 90 deg, elevation - 50 deg i.e. viewing an area of visual space on the vertical meridian in the lateral visual field, mid-way between the horizon and the lower pole of the visual field. DlSCUSSION
Our results show that, with a defined skullorientation, the geometrical centre of the eye points forward by some 15 deg from azimuth 90deg in the visual field, and downwards by 5 deg from the horizon. The skull orientation used was chosen to correspond to the head posture adopted by the pigeon during flight and walking (Hodos et al., 1984), and the characteristic head posture is probably maintained by vestibular stabilisation (Duijm, 1951). We have observed in feral pigeons, as used in this study, that this pupil-centre to beak tip angle brings the horizontal semicircular canal to the horizontal plane. How does the post-mortem eye position compare with eye position in vivo, either under anaesthesia, or in the natural state? Although the pigeon can make phasic eyemovements (Nye, 1%9), and convergent eyemovements prior to pecking (Martinoya et al.,
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B. P. HAYESer al.
Fig. 6. Perspective view of the eye cup showing the high density areas and density peaks of ganglion cells, displaced ganglion cells and centrifugal terminations. Peak densities of ganglion cells (f&d triangles) are 41,000 HRP labelled cnlls/mmz near the area centralis (asterisk) and 36,OOO/mm* towards the ccntre of the red field. Ganglion cell isodensity lines (solid lines) are 30,000 cells/mm*. The outline of the red field (r) is shown dotted; the mnainder of the retina is the yellow field (y). Peak densities of displaced ganglion cells (tilled squares) are 112 HRP labellcd cells/mm* near the area centralis and 92/mm2 in the mid-temporal retina. The 60cells/mm2 isodensity line is shown (dash-dot line). Concentrations of centrifugal fibre terminations (filled circles) are found near the centre of the eye cup (570 HRP labelled terminations/mm*) and in the mid temporal retina (440/mm2). The high density area of centrifugal terminations is delimited by the 3OO/mm’isodensity line (dashes). The approximate projections of the vertical meridian at visual field azimuth 90 deg and of the horizon (visual field elevation 0 deg) are shown by dotted lines. D, dorsal; V, ventral; N, nasal; T, temporal; p. pecten.
1984), there are several grounds for considering that the pigeon’s repertoire of eye-movements is limited. Firstly, the globe makes a tight fit in the orbit, and inside the orbit the optic nerve is short. Large eye-movements would exert undesirable traction on the optic nerve. Secondly, there is little rationale for extensive eyemovement (associated with foveation) in a panoramic eye where high cell densities are maintained over much of the retina, and high visual acuity is maintained over much of the visual field. Our experiments have shown that azimuth 0 deg in the visual field (the frontal vertical meridian) projects to the retina some 0.55-l .3 mm from the nearest oral edge, however we have not measured this at elevations below - 15 deg. This allows some 4.6-9.2 deg
overlap across the frontal meridian, with a binocular visual field of 9-l 8 deg in width, using 120 p m/deg as the peripheral retinal magnification factor. The width of the binocular field has been estimated by photography of the pupils both in anaesthetised and unanaesthetised pigeons (Martinoya et al., 1981; Jahnke, 1984). These studies give a maximal width of 30-40 deg. The width of the binocular field has been measured in anaesthetised and post-mortem pigeons, with an ophthalmoscopic method (Martin and Young, 1983) as some 28 deg. In these studies the optical measure may exceed the width of the binocular field of the retina. Even if in uiuo the binocular field is 30deg wide, this can be reconciled with our results if post mortem each eye has diverged by little more than 5 deg.
Pigeon visual field projection
There have been no studies of torsional movements of the pigeon eye during visually guided behaviour, and it would clearly be of interest to know whether these occur, or if their purpose is limited to stabilising the eye with respect to gravity. It is often assumed that the centre of the red field of the pigeon retina is related to pecking behaviour. Our observations suggest that it is not, since the frontal meridian falls outside the red field, and both the centre of the red field and its peak of ganglion cell density (Fig. 6) occur near azimuth 90 deg (in the lateral visual field). A huge torsional motion of some 90 deg could move the centre of the red field so that it viewed the ground frontally (from azimuth 30, elevation - 15 deg), and would bring the pecten close to a horizontal orientation. It seems unlikely that so large a rotation could occur, and if it did, it would entail extravagant recalibration of the central nervous system’s maps of retinal and spatial coordinates. Our observations suggest that the red field views a large elliptical patch of visual space bounded ventroanteriorly by the frontal meridian, and extending from some 10 deg below the horizon to close to the lower visual pole (dorsal retina). In flat-mounted retinae, a clear strip of yellow field extends between the red field and the ora terminalis along the dorsal margin of the red field. It should be noted that the red field exists within the myopic, lower half, of the pigeon visual field (Fitzke et al., 1985), which is conjugate to the ground-plane when the pigeon is walking or feeding. Wide jield magnification facrors
It has been calculated for the human eye that retinal magnification in the peripheral visual field is considerably reduced, by nearly twofold, in comparison with the posterior pole (Drasdo and Fowler, 1974; Fitzke, 1986). Our observations, which compare the posterior pole and the frontal periphery in the pigeon eye, suggest that in both regions the magnification factor is some 120 pm/deg. Although the optical basis for the difference remains to be investigated, it seems possible that maintenance of a constant magnification factor, and a nearhemispherical image plane, are adaptations to fine-grain panoramic vision. A previous study (Marshall et al., 1973) using a simplified Gauseye derived a retinal schematic sian magnification factor of 140 pm/deg. in the pigeon. An independent check on the value for
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peripheral magnification factor can be derived on the assumption that the visual field extends for 180deg (i.e. is a hemisphere), and that its “base” projects to the limit of the retina at the ora terminalis over a visual arc of 360 deg. Retinal magnification can then be derived as r.m.f. = ora circumference/360. We have measured the mean diameter of the ora in 12 pigeon eyes, as 13.07mm, s.d. 0.67mm. This mean diameter corresponds to a retinal magnification of 114 pm/deg which is in very reasonable accord with our experimental findings, differing by only 5%. Cell and fibre distributions In previous studies of cell and fibre distributions on retinal whole mounts (Hayes and Holden, 1983a, b) we showed that displaced ganglion cells and centrifugal terminations were concentrated in bands of retina orientated at about 70 deg to the pecten. These were considered to be horizontal on the retina. The reconstruction of an eye cup from a retinal map allows us to relate cell distribution to position in the visual field. The results show that the bands of displaced ganglion cells and centrifugal terminations are orientated at about 15 deg to the horizontal in the eye cup, and are distributed around the horizon in the visual field. Peak cell and termination densities are found close to the area centralis, equivalent to azimuth 75 deg in the visual field, and in the mid temporal eye cup, equivalent to azimuth 30-40 deg in the visual field. The displaced ganglion cell and centrifugal systems of the retina are therefore distributed to view the horizon with high acuity for the lateral and mid-frontal visual field. The ganglion cell distribution in the eye cup shows two concentrations of cells, with declining densities between them and in the periphery (Hayes, 1982). One concentration is close to the area centralis (azimuth 75 deg, near the horizon in the visual field) and a further concentration is found near the centre of the red field, corresponding to visual field azimuth 90 deg (in the lateral field), mid way between the horizon and the lower pole of the visual field. The majority of ganglion cells are found in the dorsal half of the eye cup i.e. they view the lower half of the visual field. The retinal density map of Bingelli and Paule (I 969) places the red field concentration of ganglion cells in the posterior superior quadrant and the authors conclude that this views the inferior nasal visual field
B. P. Havxs et al.
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(“pecking field”). Galifret (1968), however, places this concentration of cells much closer to the vertical meridian and describes it as an “area dorsalis”, used binocularly to view the ground. Our results show that only a narrow binocular field is present, at the temporal rim of the eye cup, and that large eye movements would be required to bring the red field cell concentration to a position for frontal binocular viewing of a “pecking field”, as recently suggested by McFadden and Reymond (1985). The ganglion cell peak in the red field occurs some 3.5 mm from the nearest ora terminalis (distance measured in retinal whole mounts). If this peak views a frontal line of sight after torsional and convergent eye movement, then a binocular field some 60 deg in width would result; this seems an implausibly large value. The concentration of ganglion cells in the red field does not therefore appear to be related to pecking bchaviour, although it might be concerned with the recognition of food grains on the ground before pecking. are grateful to the MoorfIelds Eye Hospital, the N.E.I. (U.S.A.), and to the Smith, Kline and French Foundation for financial support; and to Mr P. K. Clark for statistical advice.
Acknowledgemenrs-We
Hamdi F. A. and Whitteridge D. (1954) The representation of the retina on the optic tectum of the pigeon. Q. Ji exp. Physiol. 39, I1 l-l 19. Hayes B. P. (1982) The Structural organisation of the pigeon retina. Prog. Ref. Res. 1, 197-221. Hayes B. P., Fitzke F. W., Hodos W. and Holden A. L. (1987) A morphological analysis of experimental myopia in young chickens. Invesr. Ophthai. aisual Sci. In press. Hayes B. P. and Holden A. L. (1983a) The distribution of displaced ganglion cells in the retina of the pigeon. Expl Bruin Res. 49, 181-188.
Hayes B. P. and Holden A. L. (1983b) The distribution of centrifugal terminals in the pigeon retina. Expi Brain Res. 49, 189-197. Hodos W., Bessette B. B., Macko K. A. and Weiss S. R. B. (1985) Normative data for pigeon vision. Vision Res. 25, 1525-1527. Hodos W., Erichsen J. T., Bessette B. B. and Phillips S. J. (1984) Head orientation in pigeons: postural, locomotor and visual determinants. Neurosci. Absrr 10, 397.
Holden A. L. (1982) Electrophysiology of the avian retina. Prog. Ret. Res. 1, 179-196. Jahnke H. J. (1984) Binocular visual field differences among various breeds of pigeons. Bird Beha? S, 96-102. Marshall J., Mellerio J. and Palmer D. A. (1973) A schematic eye for the pigeon. Vision Res. 13.2449-2453. Martin G. R. and Young S. R. (1983) The retinal binocular field of the pigeon (Columba lick: English racing homer). Vision Res. 23, 911-915.
Martinoya C., Le Houezec J. and Bloch S. (1984) Pigeon’s eyes converge during feeding: evidence for frontal binocular fixation in a lateral-eyed bird. Neurosci. Len. 45, 335-339.
REFKRENCKS Bingelli R. L. and Paule W. J. (1969) The pigeon retina: quantitative aspects of the optic nerve and ganglion cell layer. J. camp. Neural. 137, I-18. Clarke P. G. H. and Whitteridge D. (1976) The projection of the retina, including the “red area” on to the optic tectum of the pigeon. Q. JI exp. Physiol. 61, 351-358. Drasdo N. and Fowler C. W. (1974) Non-linear projection of the retinal image in a wide-angle schematic eye. Br. J. Ophthal.
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Duijm M. (1951) On the head posture in birds and its relation to some anatomical features. I. Proc. Ned. Ak. Wer. C. 54, 202-211.
Fitzke F. W. (1986) A representational Modelling
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Hughes A.). Cambridge Univ. Press. Fitzke F. W., Hayes B. P., Hodos W., Holden A. L. and Low J. C. (1985) Refractive sectors in the visual field of the pigeon eye. J. Physiol. 369, 33-44. Galifret Y. (1968) Les diverses sires fonctionelles de la retine du pigeon. Z. Zellforsch. 86, 535-545.
Martinoya C., Rey J. and Bloch S. (1981) Limits of the pigeon’s binocular field and direction for best binocular viewing. Vision Res. 21, 1197-1200. McFadden S. A. and Reymond L. (1985) A further look at the binocular visual field of the pigeon (Columbu liuia). Vision Res. 25, 1741-1746. Meyer D. B. (1977) The avian eye and its adaptations. In Handbook of Sensory Physiology, Vol. VH/5, The Visual System in Vertebrates (Edited by Crescitelli F.), Chap. 10. Springer, Berlin. Nye P. W. (1969) The monocular eye movements of the pigeon. Vision Res. 9, 133-144. Pumphrey R. J. (1961) Vision, Il. In Bioiogy and Comprrratire Physiology of Birds (Edited by Marshall A. J.). Academic Press, New York. Rochon-Duvigneaud A. (1922) Une methode de determination du champ visuel chez les vertebres. Annl Oculisre 159, 56 I-570. Rochon-Duvigneaud A. (1943) Les Yeux ef la Vision des Vertebres. Masson, Paris. Stine G. H. (1934) Tables for accurate retinal localisation. Am. J. Ophthal.
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THE PROJECTION OF THE VISUAL FIELD THE RETINA OF THE PIGEON
0042-6989/87 $3.00 + 0.00 1987 PergamonJournalsLtd
UPON
B. P. HAYES, W. Horns, A. L. HOLDENand J. C. Low The Department of Visual Science, Institute of Ophthalmology, Judd St., London WC1 H9QS. England (Received 2 January 1986; in revised form 1 April 1986)
Abstract-Co-ordinates in the visual field of the pigeon eye were located in the eye cup anatomically by marking the position of the trans-scleral image. The retina1horizon and vertical meridia at azimuths 0 deg (frontal field) and 90 deg (lateral field) were located. Approximately 18 deg of binocular field are available in frontal vision and the frontal meridian projects to temporal retina outside the red field. Spatial distributions of ganglion cells, displaced ganglion cells, and centrifugal terminals were located in the eye cup. Retina1 magnification factors in the posterior pole and temporal periphery are close to 120 pm/deg. Pigeon
Visual field
Retina
Binocular vision
INTRODUCI’ION
There have been many studies of the morphology, quantitative histology and physiology of the pigeon retina (Humphrey, 1961; Meyer, 1977; Hayes, 1982; Holden 1982), of the pigeon’s visual behaviour and visual field (Rochon-Duvigneaud, 1943; Hodos et al., 1985; Martin and Young, 1983) and of the representation of the retina in the central visual pathways (Hamdi and Whitteridge, 1954; Clarke and Whitteridge, 1976). Yet little is known of the optical design of this panoramic eye, and of the design differences between a panoramic and a foveocentric optical organisation. There have been few attempts to link the spatal distribution of retinal cell types to the way the eye is aligned in, and provides a view of, the visual field. Such an analysis could provide insight into the marked regional specialisations of the pigeon retina. This paper begins such a study by relating co-ordinates of the visual field to their retinal projections, thus permitting a description of the field of view of topographical features such as the “red-field” of the retina, of the field coordinates of the pecten, and of the displaced ganglion cells and centrifugal terminals (Hayes and Holden, 1983a, 1983b). The observations are made post-mortem, using the technique of Rochon-Duvigneaud (1922) of observing the trans-scleral image of a light source. In addition to marking the co-ordinates of the visual field, our experiments provide measurements of reti-
Cell distribution
Magnification factor
nal magnification factors both in the central and the peripheral visual field. These are of some interest since it has been calculated for the human eye that there is a marked reduction in magnification in the retinal periphery (Sine, 1934; Drasdo and Flower, 1974; Fitzke, 1986) and it is natural to enquire whether this feature is found in an eye with a panoramic visual field.
METHODS
The observations were made on 10 feral pigeons, Columba livia. The animals were sacrificed under ether anaesthesia. The head was held in a stereotactic system with ear bars, and a beak bar that could be adjusted so that the beak tip was 35 deg down from the interpupillary line. A bright 20 W quartz-halogen lamp with 2mm filament (Thorn, M-20) was positioned 50 cm from the eye in a perimeter system. The bulb could be rotated about the centre of the pupil in a vertical arc through varying elevations in the visual field. Angles below the horizontal were designated as negative elevations, and above the horizontal as positive elevations. The head could be rotated about the centre of the pupil on a milling machine stand, which was equivalent to the light source being displaced in a horizontal arc through varying angles of azimuth. Azimuth Odeg in the visual field was defined as frontal, parallel to the saggital plane of the head. These perimeter motions define a 31
B. P. HAYESet al.
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simple co-ordinate system for the visual field of each eye, directly analogous to the cartographical coordinates of the earth; lines of iso-elevation are equivalent to the lines of latitude, and lines of constant azimuth (vertical meridia) are equivalent to the lines of longitude. A visual pole occurs at the upper and lower visual field, where the meridia meet. The geographical equator is equivalent to the visual horizon. A diagrammatic view of the visual field co-ordinates is given in Fig. l(a). The head was dissected to expose a limited region of the sclera of the left eye, centred either at the fundal pole, or at the temporal periphery of the globe, for locating central field coordinates (in the region of visual field coordinates azimuth 90deg and elevation Odeg) and peripheral field coordinates (azimuth 0 deg, elevation 0 to - 70 deg), respectively. The position of the light source was adjusted, and its coordinates were noted. The trans-scleral image of the light source (Rochon-Duvigneaud, 1922) was observed under a dissecting microscope, and a cautery bum was applied to the sclera over the image, in order to mark the position of the image in the retina, through the outer coats of the eye. Three to fourteen burns were made in each eye. The lamp was usually displaced with 10deg intervals between adjacent positions, so that retinal marks were separated by approx. 1 mm. The scleral image was less easy to locate at the retinal periphery, because of the reduction in intensity due to the shape of the pupil in the periphery of the visual field.
The eye was excised and fixed in phosphate buffered 3% glutaraldehyde, as described in Hayes et al. (1987). The anterior segment and vitreous were removed and the burns were located in the eye cup. The eye cup was photographed at x 1.44 magnification. The distances between the centres of the burns were measured from prints at x 7.2 magnification, as described below. In order to facilitate comparison of the macrophotographs of eye cups, a standard perspective view was computed of the visual field co-ordinates transferred to a hemisphere 6.8 mm in radius, and imaged in the film plane of the macro-camera. The value of 6.8 mm as the radius for a standard eye cup was arrived at after curve fitting of retinal outlines with a mainframe computer (Euclid System, University College, London). Retinal outlines (at the plane of the photoreceptors) were traced from macro-photographs of hemisected eye-cups, using a bit pad for data entry. It was found that sections of the retina could be well fitted by segments of a circle, and the value of 6.8 mm was derived from three computer fitted experiments. The computation of the perspective view was carried out in a laboratory microcomputer, and plots were produced on a Hewlett-Packard 7470A plotter. The accuracy of the computer model, and the scale distortions introduced by photograph of a hemispherical cup were checked by photography of a cup containing equidistant calibration marks. Linear distance on the photograph was near-proportional to
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go,-90 D
T
.‘j i
go,-90
visual
field
go,90 v
eye
cup
Fig. 1. Diagrammatic representation of the visual field co-ordinates (a) and eye cup co-ordinates (b) used in this study. The number pairs give azimuth and elevation values, and the letters give anatomical locations in the eye cup; N, nasal; T, temporal; D, dorsal; V, ventral. The oblique outline in the temporal to ventral quadrant represents the pecten base.
Pigeon visual field
degrees of arc angle for eccentricities up t0 40 deg from the geometric centre of the cup; and the computed values agreed closely with the measured distances. It should be noted that eye cup co-ordinates are displaced from the visual field co-ordinates. They would correspond exactly only if visual field co-ordinate elevation 0 deg, azimuth 90 deg projected exactly to the geometrical centre of the eye cup. A diagrammatic view of the eye cup co-ordinates is given in Fig. l(b). The positions of retinal marks and the pecten, area centralis and outline of the red field were drawn onto computer plots of the standard perspective view of the eye cup by projecting macrophotographs in an enlarger. The enlarger magnification was varied to match the rim of the eye cup with the outline of the computer plot and the orientation adjusted to bring the pecten to an angle of 72 deg to the horizontal, which is the pecten angle in the alert, unrestrained, pigeon, (Hayes and Holden, 1983a) and the pecten angle observed when the bill is held 35 deg down in the stereotactic instrument. Retinal magnification factors @m of retinal distance/degree arc in the visual field) were calculated. Distance between the centres of retinal marks was measured on the eye-cup photographs. Retinal distances were measured near the geometrical centre of the whole eye cup as straight-line distances on the photograph. Where marks were close to the edge of the eye-cup, the cup was bisected so that its oral edge could be rotated to be viewed axially at the centre of the photograph, where the representation of the curved surface most closely approximated to Retinal planar geometry. magnification factors were calculated as the ratio of retinal arc length to the angle subtended in the visual field (pm per degree). Arc length in the visual field was computed from the visual field co-ordinates noted during the experiment as: arc = cos-’ [(sin a* sin b)
where the symbol * indicates multiplication, a and b are the elevations associated with two readings, and P is their difference in azumuth. Retinal arc length was computed assuming that the retinal surface is spherical, and of radius 6.8 mm. In order to compare cell and fibre distributions in the retina with visual field co-ordinates
projection
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a single retinal map incorporating isodensity lines of ganglion cell, displaced ganglion cell and centrifugal terminal distributions and retinal landmarks was made from the data of Hayes and Holden (1983a, b). The map of the flat-mount was reconstructed into a cup shape by taping together the edges that represent the cuts made before the retina was flattened. The reconstruction was then photographed with the macrocamera. The negative was projected to fill a computer plotted perspective view of the eye cup and the pecten angle adjusted to 72 deg. The isodensity lines and retinal landmarks were then transferred to the perspective view of the eye cup. RESULTS
(1) The appearance of the retinal marks Electrocautery produced pits of approx. 0.7mm diameter in the external surface of the sclera. On examination of the eye cup the macroscopic appearance of the fundus was well preserved and the pecten, red field and sometimes the pit of the area centralis could be seen (Fig. 2). Seventy-seven percent of the bums produced a mark on the retina, clearly discemible in the eye cup (Figs 2 and 3). The majority of retinal marks consisted of a nearly circular central white area of mean diameter 0.8 f 0.3 mm (n = 50) surrounded by a narrow grey halo of 0.2 &-0.04 mm (n = 28) mean width. Occasionally only a grey mark of 0.5 to 0.8 mm diameter was seen. When a scleral burn did not produce a mark on the retina a fine insect pin (0.15 mm diameter) was inserted perpendicular to the sclera, through the centre of the scleral pit. This produced a fine tear in the retina extending for about 0.5 mm. The centres of retinal marks were taken as the intersection of two diameters mutually at right angles. Posterior retina marks (of which 49 were recovered) were distributed in a nearly square grid over the central 10% of the retinal area (Fig. 2). Temporal retinal marks (Fig. 3) (46 were recovered) were not so evenly distributed; they were in a nearly square grid near the horizontal meridian but they showed horizontal convergence at decreasing elevation in the visual field. (2) The location of the horizon and vertical meridia Retinal marks were plotted onto computer generated perspective views of the eye cup (e.g.
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B. P. H Am
Fig. 4). Horizon marks (visual field elevation 0 deg) were found to lie approximately parallel to the horizontal grid lines at eye cup corordinates + 5 deg elevation. Marks at azimuth 90 deg in the visual field were nearly parallel to the vertical grid lines at eye cup co-ordinates azimuth 105 deg. This azimuth 90 deg, elevation Odeg, in the visual field i.e. lateral to the head and at the level of the pupil, projected approx. 15 deg nasal and 5 deg ventral to the centre of the eye cup (Fig. 4). This was about 17 deg nasal to the position of the area centralis. As can be seen in Fig. 4, marks made at azimuth 0 deg in the visual field were found parallel to the temporal edge of the eye cup, at about 15 deg from the rim (Fig. 4) (cup coordinates azimuth 15 deg) and just outside the temporal edge of the red field. The red field was an elliptical area in the dorsal third of the eye cup (Fig. 4) and a single mark made at visual field co-ordinates azimuth 85 deg, elevation - 60 deg was located near its centre. The head of the pecten was found to be located at 20 deg temporal and 10 deg ventral to the centre of the eye cup (Fig. 4).
et al.
(3) The margins and extent of the visual field Marks made at azimuth Odeg in the visual field, i.e. with the lamp positioned directly in front of the head, were found to lie within 10-20 deg of the rim of the eye cup (Fig. 4). A narrow band of temporal retina is therefore available for binocular overlap of the frontal visual field. The width of this binocular region, measured from the ora serrata, varied between 1.3 mm at -30 deg elevation and 0.55 mm at - 70 deg elevation (Fig. 3). (4) Retinal ~agn~~~tio~ in the v~~a~~eld Measurements of retinal magnification factors are summarised in the histograms shown in Fig. 5. Measurements taken at the posterior pole of the eye are shown in Fig. 5(a), based on 203 readings, and measurements taken in the temporal periphery (in the region of azimuth 0 deg in the visual field) are shown in Fig. 5(b), based on 164 readings. The mean retinal magnification at the posterior pole was 119.27 pm, standard deviation 12.38 pm: at the retinal periphery the mean temporal 0
Fig. 4. Perspective view of the eye cup (grid lines are 10 deg apart) showing marks of the vertical mcridia, horizon and retinal features, The outline of the red field (r) is shown dotted. Solid circles: azimuth 90 deg marks; solid squares: elevation Odeg marks; solid triangles: azimuth Odeg marks; open circle: md field mark at azimuth 85, elevation -60. The approximate projections of the vertical meridian at visual fieId azimuth 90 deg and of the horizon (visual field elevation 0 deg) are shown by dotted tines. D, dorsal; Y, ventral; N, nasat; T, temporal; p, pecten; y, yellow field.
Fig. 2. Macro-photograph of an eye cup showing marks on the retina which resulted from 10 scleral bums spaced 10deg apart, near the centre of the visual field (azimuth 70-100, elevation IO to -2Odeg). The centres of the marks from which measurements were taken are shown (dots). Numbers indicate the visual field co-ordinates of the light source. A retinal detachment (d) in the naso-temporal periphery occurred during dissection. The red field (r, outline dotted) appears paler than the yellow field (y). D, dorsal; V, ventral; N, nasal; T, temporal; p, pecten. Scale line: 1 mm.
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Fig. 3. Macro-photograph of the temporal half of an eye cup from an eye which received 13 scleral bums in the temporal peripheral retina spaced lOdeg apart in visual space (azimuth C-30, elevation -20 to - 70 deg). Numbers indicate the visual co-ordinates of the light source. The cup has been tilted to bring the marks close to the camera axis for measurement of distances on the retina (dots show the centres of the marks). The diameter of the marks is 0.5-l .4 mm. D, dorsal; V, ventral; r, red field (outline dotted); p, pecten; n, optic nerve; 0, ora serrata. Scale line: I mm.
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37
Pigeon visual field projection 50
r
(a)
(b)
r Fig. 5. Histograms of retinal magnification factors. Abscissa, magnification factor, (Ctm/deg); ordinate, percentage frequency. Histogram (a) derived from measurements at the posterior pole of the eye; histogram (h) derived from measurements at the temporal periphery.
magnification was 119.47 pm, standard deviation 16.62pm. These means are not significantly different using Student’s r-test: (given the sample sizes and variances, a difference in mean of f 1.5 pm would be statistically significant at the 0.05 level). The two distributions are not significantly different using the Mann-Whitney U-test. Thus retinal magnification is essentially identical in the central and the peripheral visual field of the pigeon eye. (5) Reconstruction of cell and terminal distributions in the retina The distribution maps of ganglion cells, displaced ganglion cells and centrifugal terminals
were reconstructed onto a perspective view of the eye cup, and are illustrated in Fig. 6. Bands of high density of displaced ganglion cells and centrifugal terminals were found near the horizontal meridian of the eye cup, and the visual horizon, and they were oriented at approx. 15 deg to the horizontal grid. These bands extended from the posterior pole to the mid temporal region of the eye cup. Within the bands of high density concentrations of ganglion cells, displaced ganglion cells and centrifugal terminals were found near the centre of the cup at cup co-ordinates azimuth 85-95 deg, elevation 0-10deg. This area of the cup views the visual field close to the horizon, near visual field azimuth 75 deg. Concentrations of displaced ganglion cells and centrifugal terminals also occur in the mid temporal retina near the horizon, and these view the frontal visual field just below the horizon at azimuth 30-40 deg, elevation -5 to - 10 deg. High densities of ganglion cells are found near the centre of the eye cup, with a peak density adjacent to the fovea. Figure 6 also includes a reconstructed outline of the red field, which matches that found by macro-photography. Towards the centre of the red field a concentration of ganglion cells is found at visual field co-ordinates azimuth 90 deg, elevation - 50 deg i.e. viewing an area of visual space on the vertical meridian in the lateral visual field, mid-way between the horizon and the lower pole of the visual field. DlSCUSSION
Our results show that, with a defined skullorientation, the geometrical centre of the eye points forward by some 15 deg from azimuth 90deg in the visual field, and downwards by 5 deg from the horizon. The skull orientation used was chosen to correspond to the head posture adopted by the pigeon during flight and walking (Hodos et al., 1984), and the characteristic head posture is probably maintained by vestibular stabilisation (Duijm, 1951). We have observed in feral pigeons, as used in this study, that this pupil-centre to beak tip angle brings the horizontal semicircular canal to the horizontal plane. How does the post-mortem eye position compare with eye position in vivo, either under anaesthesia, or in the natural state? Although the pigeon can make phasic eyemovements (Nye, 1%9), and convergent eyemovements prior to pecking (Martinoya et al.,
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B. P. HAYESer al.
Fig. 6. Perspective view of the eye cup showing the high density areas and density peaks of ganglion cells, displaced ganglion cells and centrifugal terminations. Peak densities of ganglion cells (f&d triangles) are 41,000 HRP labelled cnlls/mmz near the area centralis (asterisk) and 36,OOO/mm* towards the ccntre of the red field. Ganglion cell isodensity lines (solid lines) are 30,000 cells/mm*. The outline of the red field (r) is shown dotted; the mnainder of the retina is the yellow field (y). Peak densities of displaced ganglion cells (tilled squares) are 112 HRP labellcd cells/mm* near the area centralis and 92/mm2 in the mid-temporal retina. The 60cells/mm2 isodensity line is shown (dash-dot line). Concentrations of centrifugal fibre terminations (filled circles) are found near the centre of the eye cup (570 HRP labelled terminations/mm*) and in the mid temporal retina (440/mm2). The high density area of centrifugal terminations is delimited by the 3OO/mm’isodensity line (dashes). The approximate projections of the vertical meridian at visual field azimuth 90 deg and of the horizon (visual field elevation 0 deg) are shown by dotted lines. D, dorsal; V, ventral; N, nasal; T, temporal; p. pecten.
1984), there are several grounds for considering that the pigeon’s repertoire of eye-movements is limited. Firstly, the globe makes a tight fit in the orbit, and inside the orbit the optic nerve is short. Large eye-movements would exert undesirable traction on the optic nerve. Secondly, there is little rationale for extensive eyemovement (associated with foveation) in a panoramic eye where high cell densities are maintained over much of the retina, and high visual acuity is maintained over much of the visual field. Our experiments have shown that azimuth 0 deg in the visual field (the frontal vertical meridian) projects to the retina some 0.55-l .3 mm from the nearest oral edge, however we have not measured this at elevations below - 15 deg. This allows some 4.6-9.2 deg
overlap across the frontal meridian, with a binocular visual field of 9-l 8 deg in width, using 120 p m/deg as the peripheral retinal magnification factor. The width of the binocular field has been estimated by photography of the pupils both in anaesthetised and unanaesthetised pigeons (Martinoya et al., 1981; Jahnke, 1984). These studies give a maximal width of 30-40 deg. The width of the binocular field has been measured in anaesthetised and post-mortem pigeons, with an ophthalmoscopic method (Martin and Young, 1983) as some 28 deg. In these studies the optical measure may exceed the width of the binocular field of the retina. Even if in uiuo the binocular field is 30deg wide, this can be reconciled with our results if post mortem each eye has diverged by little more than 5 deg.
Pigeon visual field projection
There have been no studies of torsional movements of the pigeon eye during visually guided behaviour, and it would clearly be of interest to know whether these occur, or if their purpose is limited to stabilising the eye with respect to gravity. It is often assumed that the centre of the red field of the pigeon retina is related to pecking behaviour. Our observations suggest that it is not, since the frontal meridian falls outside the red field, and both the centre of the red field and its peak of ganglion cell density (Fig. 6) occur near azimuth 90 deg (in the lateral visual field). A huge torsional motion of some 90 deg could move the centre of the red field so that it viewed the ground frontally (from azimuth 30, elevation - 15 deg), and would bring the pecten close to a horizontal orientation. It seems unlikely that so large a rotation could occur, and if it did, it would entail extravagant recalibration of the central nervous system’s maps of retinal and spatial coordinates. Our observations suggest that the red field views a large elliptical patch of visual space bounded ventroanteriorly by the frontal meridian, and extending from some 10 deg below the horizon to close to the lower visual pole (dorsal retina). In flat-mounted retinae, a clear strip of yellow field extends between the red field and the ora terminalis along the dorsal margin of the red field. It should be noted that the red field exists within the myopic, lower half, of the pigeon visual field (Fitzke et al., 1985), which is conjugate to the ground-plane when the pigeon is walking or feeding. Wide jield magnification facrors
It has been calculated for the human eye that retinal magnification in the peripheral visual field is considerably reduced, by nearly twofold, in comparison with the posterior pole (Drasdo and Fowler, 1974; Fitzke, 1986). Our observations, which compare the posterior pole and the frontal periphery in the pigeon eye, suggest that in both regions the magnification factor is some 120 pm/deg. Although the optical basis for the difference remains to be investigated, it seems possible that maintenance of a constant magnification factor, and a nearhemispherical image plane, are adaptations to fine-grain panoramic vision. A previous study (Marshall et al., 1973) using a simplified Gauseye derived a retinal schematic sian magnification factor of 140 pm/deg. in the pigeon. An independent check on the value for
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peripheral magnification factor can be derived on the assumption that the visual field extends for 180deg (i.e. is a hemisphere), and that its “base” projects to the limit of the retina at the ora terminalis over a visual arc of 360 deg. Retinal magnification can then be derived as r.m.f. = ora circumference/360. We have measured the mean diameter of the ora in 12 pigeon eyes, as 13.07mm, s.d. 0.67mm. This mean diameter corresponds to a retinal magnification of 114 pm/deg which is in very reasonable accord with our experimental findings, differing by only 5%. Cell and fibre distributions In previous studies of cell and fibre distributions on retinal whole mounts (Hayes and Holden, 1983a, b) we showed that displaced ganglion cells and centrifugal terminations were concentrated in bands of retina orientated at about 70 deg to the pecten. These were considered to be horizontal on the retina. The reconstruction of an eye cup from a retinal map allows us to relate cell distribution to position in the visual field. The results show that the bands of displaced ganglion cells and centrifugal terminations are orientated at about 15 deg to the horizontal in the eye cup, and are distributed around the horizon in the visual field. Peak cell and termination densities are found close to the area centralis, equivalent to azimuth 75 deg in the visual field, and in the mid temporal eye cup, equivalent to azimuth 30-40 deg in the visual field. The displaced ganglion cell and centrifugal systems of the retina are therefore distributed to view the horizon with high acuity for the lateral and mid-frontal visual field. The ganglion cell distribution in the eye cup shows two concentrations of cells, with declining densities between them and in the periphery (Hayes, 1982). One concentration is close to the area centralis (azimuth 75 deg, near the horizon in the visual field) and a further concentration is found near the centre of the red field, corresponding to visual field azimuth 90 deg (in the lateral field), mid way between the horizon and the lower pole of the visual field. The majority of ganglion cells are found in the dorsal half of the eye cup i.e. they view the lower half of the visual field. The retinal density map of Bingelli and Paule (I 969) places the red field concentration of ganglion cells in the posterior superior quadrant and the authors conclude that this views the inferior nasal visual field
B. P. Havxs et al.
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(“pecking field”). Galifret (1968), however, places this concentration of cells much closer to the vertical meridian and describes it as an “area dorsalis”, used binocularly to view the ground. Our results show that only a narrow binocular field is present, at the temporal rim of the eye cup, and that large eye movements would be required to bring the red field cell concentration to a position for frontal binocular viewing of a “pecking field”, as recently suggested by McFadden and Reymond (1985). The ganglion cell peak in the red field occurs some 3.5 mm from the nearest ora terminalis (distance measured in retinal whole mounts). If this peak views a frontal line of sight after torsional and convergent eye movement, then a binocular field some 60 deg in width would result; this seems an implausibly large value. The concentration of ganglion cells in the red field does not therefore appear to be related to pecking bchaviour, although it might be concerned with the recognition of food grains on the ground before pecking. are grateful to the MoorfIelds Eye Hospital, the N.E.I. (U.S.A.), and to the Smith, Kline and French Foundation for financial support; and to Mr P. K. Clark for statistical advice.
Acknowledgemenrs-We
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