Exp Brain Res (1981) 44:431-436 _Experimental .Bran Research �9 Springer-Verlag 1981

Research Note

Topographic Organization of Orientation Columns in the Cat Visual Cortex

A Deoxyglucose Study

W. Singer

Max-Planck-Institute for Psychiatry, Kraepelinstr. 2, D-8000 Munich 40, Federal Republic of Germany

Summary. Three-dimensional reconstructions of the orientation column system were obtained from the visual cortex of four cats using the deoxyglucose technique. One cat had normal visual experience, one was monocularly deprived and two had selective experience with vertical and horizontal contours, respectively. In areas 17 and 18 orientation columns form a remarkably regular system of equally spaced parallel bands whose trajectory is orthogonal to the borderline between areas 17 and 18. This topo- graphic organization is resistant to manipulations of early visual experience.

Key words: Cat - Visual cortex - Orientation col- umns - Deoxyglucose

Hubel et al. (1977, 1978) have demonstrated for the monkey striate cortex and a number of subsequent investigators for the visual system of the cat (Stryker et al. 1977; Albus 1979; Flood and Coleman 1979; Singer et al. 1981) and the tree shrew (Skeen et al. 1978), that the orientation column system can be mapped by autoradiographic determination of local glucose consumption (Sokoloff et al. 1977). The objective of the present study was to investigate the topographic organization of the orientation column system in cat by three-dimensional reconstructions of orientation columns in areas 17 and 18. While the present manuscript was in preparation, a paper appeared by Humphrey et al. (1980) in which they describe results very similar to ours for the striate cortex of the tree shrew.

The experimental procedures for deoxyglucose- mapping were the same as described in detail previ- ously (Singer et al. 1981). In brief, lightly anes- thetized and paralyzed cats were injected i.v. with 200 ~C/kg of C14-deoxyglucose and stimulated for

50 min either with a horizontal or a vertical grating pattern of continuously varying spatial frequency which drifted over a projection screen in front of the animal. After rapid freezing of blocks containing the occipital pole of the cerebral hemispheres 30 ~tm thick serial sections were prepared and all sections were exposed for 3 weeks at -60 C ~ to high resolu- tion mammography film (Mammoray TR Agfa). One hemisphere (from cat C1) was cut parallel to the frontal plane, all others were cut parallel to the horizontal plane. After exposure the sections were counterstained with Thionin for determination of

a rea boundaries. For three-dimensional reconstruc- tion the enlarged autoradiographs were copied on transparent perspex sheets and these were mounted between plates whose thickness matched the distance between the serial sections and the magnification factor of the drawings. To make sure that the selection of serial sections - even though it always occurred according to a fixed schedule - did not introduce distortions of the columnar pattern, recon- structions were also made from the discarded sec- tions. These revealed a pattern virtually identical to that of the models represented in Figs. 2 and 3. The tracks of three needles inserted into the blocks prior to freezing served as guidelines for correct superposi- tion. Reconstructions were made from the visual cortex of four animals. One had normal visual experience during early development, one was monocularly deprived from birth and two had experi- enced only vertical or horizontal orientations, respec- tively, wearing -25 dioptr, cylindrical lenses in front of both eyes whenever leaving the dark room. The latter two cats had been subjects of a previous study (Singer et al. 1981). The raising conditions and the stimulus configurations used for deoxyglucose map- ping are summarized in Table 1.

Horizontal sections through the dorsal crest of the lateral gyrus are tangential to the cortical lamina-

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Table 1

W. Singer: Orientation Columns

Kitten No. Raising condition Age at experiment Stimulation condition Dosage of label

C1 Normal visual 12 weeks Binocular, 200 ~C/kg/C14 experience vertical contours,

stimulus velocity 5~

C2 Monocular deprivation 12 weeks Monocular through experienced 200 btC/kg/C14 from 2 weeks of age eye, vertical contours,

stimulus velocity: 5 ~ and 15~ in alternation

C3 1 Dark rearing until 7 weeks [C3] Binocular, 200 ~tC/kg/C14 day 28, subsequently horizontal [C3] or

C4 > 200 h of selective 8 weeks [C4] vertical [C4] contours, stimulus experience, with vertical velocity 5 ~ and 15~ in [C3] or horizontal alternation [C4] contours

tion in an area where the vertical meridian and hence the borderline between areas 17 and 18 is repre- sented. In autoradiographs from these sections zones of increased optical density appear as fairly parallel bands whose spacing is in the order of 1 mm, and whose main orientation is orthogonal to the repre- sentation of the vertical meridian (Fig. 1). Deeper sections are orthogonal to the cortical lamination and here zones of increased optical density appear as regularly spaced columns which are orthogonal to the cortical surface and in most cases continuous throughout all cortical laminae. On occasions, how- ever, these columns are confined to only deep or superficial laminae and whenever such is the case for several adjacent columns, deep and superficial densities are out of register (Fig. 1).

The reconstructions of serial sections from the two cats (C1, C2) which had unrestricted contour vision demonstrate that the bands of increased opti- cal density actually continue from the dorsal crest of the lateral gyrus down the medial bank, uninter- rupted trajectories of up to 6 mm being quite com- mon (Fig. 2). The bands remain parallel to the frontal plane and the average distance between them stays in the order of I mm throughout striate cortex. Only in the most posterior portions of area 17 the bands take a more rostro-caudal course. This might suggest that they tend to run orthogonal also with respect to the outer boundaries of striate cortex. As expected from this organization of iso-orientation bands, distinct columns of increased activity were distinguishable only in the most caudal and rostral sections of the block which was cut in the frontal plane.

Two characteristic disturbances of this regular pattern are commonly observed: First, the intercala- tion of additional, blind ending bands and second,

the confluence of two adjacent bands. Such irre- gularities appear to be particularly frequent on the dorsal crest of the lateral gyrus close to the border- line between areas 17 and 18 (Fig. 1). Comparison of individual sections with the reconstructed trajectories indicates that blind ending bands are the major cause for the sometimes incomplete translaminar extent of columns. Probably because sections are only rarely parallel to the edge of blind ending bands the latter appear to start either in supra- or infragranular layers and to gradually increase in depth until they finally extend throughout all laminae. Such irregularities, if present also close to the vertical meridian in monkey striate cortex, are probably the cause of the scatter of preferred orientations, that was noted by Bauer et al. (1980) along recording penetrations which were close to the foveal representation.

As described in detail previously (Singer et al. 1981) in the two cats which had experienced only horizontal (C3) or vertical (C4) contours glucose consumption was determined while one hemisphere was stimulated with the same orientation as that experienced previously and the other hemisphere was stimulated with the orthogonal orientation. On the side stimulated with the orientation which corre- sponded to previous experience columns were broader than on the other side and tended to merge with each other, in particular outside layer IV. In the hemisphere stimulated with the grating whose orien- tation was orthogonal to that experienced previously zones of increased activity were narrow and essen- tially confined to layer IV. Reconstructions were made only from these hemispheres since only here zones of increased activity were sufficiently well seggregated. The dark zones in the reconstructions are thus corresponding to activity which is restricted essentially to layer IV and is from units which

W. Singer: Orientation Columns 433

Fig. 1, Autoradiographs and Nissl preparations of serial sections from visual cortex of kitten C1. This kitten had normal visual experience and for deoxyglucose-mapping was stimulated binocularly with vertically oriented contours. The sections are parallel to the horizontal plane, their distance from the dorsal crest is indicated below each autoradiograph. Superficial sections are tangential to the cortical lamination and comprise the border region between areas 17 and 18. The representation of the vertical meridian corresponds approximately to the line between the two needle holes indicated by arrows in the Nissl stained section A4. Deeper sections are orthogonal to the cortical lamination and contain area 17 on the medial bank of the lateral gyrus and area 18 on the medial bank of the lateral sulcus. Zones of increased optical density correspond to the clustering of neurones responsive to vertically oriented contours. In sections tangential to the cortical lamination these zones appear as bands whose orientation tends to be perpendicular to the representation of the vertical meridian. The arrows in the autoradiograph A2 indicate two bands which merge with each other in the vicinity of the 17/18 border and the arrow in autoradiograph A4 indicates the beginning of a new band. In the deeper sections which are orthogonal to the cortical lamination zones of increased optical density appear as regularly spaced columns whose spacing is in the order of 1 mm. Most of these columns extend throughout all laminae but on occasions they may be confined to superficial or deep layers only (arrow in autoradiograph A6). To increase the contrast of columns and to reduce the noise of background activity, autoradiographs from two adjacent sections were superimposed for these reproductions. The arrows in the Nissl stained sections A4 to A6 indicate the holes from the needle tracks which served as guidelines for later reconstruction

434 W. Singer: Orientation Columns

Fig. 2. Three-dimensional reconstruction of the orientation column system in area 17 of four cats (C1 to C4). The reconstructions show the medial bank of the lateral gyrus and comprise exclusively area 17. Kitten C1 had normal visual experience and for deoxyglucose-mapping was stimulated binocularly with vertical contours. Kitten C2 was monocularly deprived and stimulated through the normal eye with vertical contours. Kitten C3 had experienced only vertically oriented contours and the reconstructed hemisphere was stimulated with horizontal contours; kitten C4 had experienced horizontal contours and the reconstructed hemisphere was stimulated with vertical contours. The magnification factor of the serial sections is the same in all reconstructions. Since less tissue was available from the brains of kittens C3 and C4 the dorso-ventral scale has been doubled in these two reconstructions. The reconstructions C1, C2 contain 75 plates, each, and the reconstructions C3, C4 contain 65 plates, each. Abbreviations: SSPL = suprasplenial sulcus; SPL = splenial sulcus; APO = zero frontal plane. Further descriptions are given in the text

r e s p o n d to a n o r i e n t a t i o n o r t h o g o n a l to t h a t e x p e r i -

e n c e d p r e v i o u s l y . A s s h o w n in Fig. 2 t h e t o p o g r a p h i -

cal a r r a n g e m e n t o f cel ls r e s p o n s i v e to t h i s o r i e n t a t i o n

is v i r t u a l l y i d e n t i c a l to t h a t f o u n d in ca t s w h i c h h a d

n o r m a l c o n t o u r v i s i on . I n k i t t e n C3 t h e b a n d s a p p e a r

tO b e e v e n m o r e r e g u l a r t h a n in ca t s C1 a n d C2 w h o

h a d n o r m a l c o n t o u r v i s i o n .

I n t w o ca t s (C3 , C4) t h e t o p o g r a p h y o f o r i e n t a -

t i o n c o l u m n s c o u l d b e d e t e r m i n e d a l so in a r e a 18. I n

a r e a 18 o f k i t t e n C1 c o l u m n s o f i n c r e a s e d ac t i v i t y

Fig. 3. Three-dimensional reconstructions of the orientation column system in the medial bank of the postero-lateral sulcus of cats C3 and C4. The reconstructions are from the same hemispheres and from the same sections that served for the reconstruction of area 17 in Fig. 2. In these two cats the 17/18 border was on the dorsal crest of the lateral gyrus and took a similar course as in C1. Hence, the reconstructions show only area 18

W. Singer: Orientation Columns 435

Fig. 3 2mm

2mm

436 W. Singer: Orientation Columns

were not sufficiently well distinguishable, probably because this cat had been stimulated only with slowly moving contours (Table 1). In kitten C2 columns were clearly visible in area 18, but an irregular curvature of the postero-lateral sulcus made the reconstruction of area 18 with the present technique impossible. As in area 17 regularly spaced, parallel bands of increased optical density are distinguishable also in area 18. They are parallel to the frontal plane and hence again orthogonal to the 17/18-border (Fig. 3). Patches of increased activity were present also in the other visual areas but here the width of individual columns, the intercolumnar distance and the variability of these parameters were considerably greater than in area 17. Because of the complicated geometrical arrangement of these areas no recon- struction was at tempted.

In conclusion, the present results demonstrate that in areas 17 and 18 of the cat, cells with similar orientation preferences are aligned in bands whose main trajectory is orthogonal to the representat ion of the vertical meridian and probably also orthogonal to the outer boundaries of the two areas. Together with the finding that blind endings are particularly fre- quent in the vicinity of the vertical meridian this suggests that area boundaries might subserve a special function in structuring the columnar pattern. The topographical organization of iso-orientation bands is remarkably constant across individuals and is resistant to manipulations of early visual experi- ence such as monocular deprivation and restriction of contour vision. Thus, columnar periodicity appears to be an intrinsic proper ty of cortical organization which is at best modifiable by experience but whose expression does not require instructions f rom the outer world. Shatz et al. (1977) have reported that in cat ocular dominance columns, too, are orthogonal to the 17/18 border and have a periodicity of about 1 mm. The two columnar systems thus appear to share the basic features of organization suggesting perhaps a common organizational principle for the generation of columnar arrangements in general.

The present results closely resemble those obtained by Humphrey et al. (1980) in the tree shrew but differ in some aspects f rom those described for the rhesus monkey by Hubel et al. (1977, 1978). The orientation columns in the macaque striate cortex appear to be organized in a more complex way, parallel bands, if visible at all, are shorter and coexistent with more randomly distributed circum- scribed patches. Humphrey et al. (1980) argued that this difference might result f rom the fact that the monkey possesses in addition a system of ocular

dominance columns while the tree shrew does not. Since the cat does have a well developed system of ocular dominance columns, additional causes for this apparent difference between macaques on one side and cats and tree shrews on the other may have to be considered. One possibility is that other features such as spatial frequency or colour are also mapped in columnar systems which are superimposed on the orientation bands. If these additional maps are more distinct in primates than in the cat, and if the stimulus used in the deoxyglucose experiment does not con- tain these additional features in a uniform distribu- tion, orientation bands may appear as less continuous in the primate than in the cat.

Acknowledgements. I wish to thank Susanne Zieglgfinsberger for her competent technical assistance in the experiments and the reconstructions and Mariele Kremling for editing the manuscript.

References

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Received July 13, 1981 / Accepted September 30, 1981