Alternating afferent zones of high and low axon terminal density within the macaque motor cortex

Brain Research, 106 (1976) 365-370 © Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands

365

Short Communications

Alternating afferent zones of high and low axon terminal density within the macaque motor cortex

HEINZ KtJNZLE Institutefor Brain Research, Universityof Zurich, 8029 Zurich (Switzerland) (Accepted January 19th, 1976)

While the radial organization of the cerebral cortex is already well established 4,10,1a,14, the existence of subunits (columns, zones, colonies or slabs) and their possible interrelationship are still rather controversia115,16. There is considerable disagreement between the various physiological reports~,Z,6,9,~, ~z, in particular with respect to the motor cortex, and the anatomical data are sparse a,7,16. The present autoradiographic analysis will demonstrate that apart from the well-known somatotopic organization a vertically oriented alternating arrangement of zones may exist in the terminal organization of cortico-cortical afferents. The investigation was made on the same 7 monkeys (Macaca fascicularis) as described in detail recentlya. The results were mainly drawn from experiment 72451, where one single injection was placed in the precentral 'leg' region (area 4) by applicating 5.2/~1 [aH]proline (total activity 50/zCi) with a syringe needle (inner diameter 0.1 mm) driven by a micromanipulator over a period of 4 h. The survival time was 8 days. The characteristic pattern of termination was most clear in areas 4 and 6 of the contralateral cortex, where the commissural fibres ended in a strikingly discontinuous pattern (Figs. 1 and 2). There were up to 13 patches of silver grain accumulations of varying density, often band-like and lying perpendicular to the surface. These bands stretched from the surface to the depth of the cortex although layers I, III and VI were most heavily covered with silver grains. The band width varied between 2001300/~m; however, occasionally it could extend up to 2500/zm when an adjacent region of much lower density was included (e.g., Fig. 1, section 3, band d). No clear relationship could be found between band width and band density. Bands were most numerous in the homotopic cortical region contralateral to the injection field and they were in general of higher density. The bands were separated by a variable interspace of a few to up to 2000/~m (5000/~m as far as the two most lateral bands are concerned), and its width was independent of the size of the adjacent band. The interspace was characterized by a

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Fig. 1. Drawing from frontal sections of exp. 72-451 showing a discontinuous, vertically oriented or band-like grain pattern in the precentral cerebral cortex (cmgular, primary and secondary motor areas) and more horizontally oriented grain accumulatnons in the primary sensory cortex. Band-like grain arrangements are separated from each other by a grain-free or faintly labelled interspace. The bands b-n on the contralateral side of sections 2-4 refer to the zones reconstructed in Fig. 3 The grain density was judged according to a 5-point subjective rating scale. The region labelled by a question mark could not be investigated, ce, sulcus eentralis, la, sutcus lateralis, ]p, sulcus intraparietalis.

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Fig. 2. Composite photograph of dark-field autoradiographs demonstrating the &scontinuous gram pattern m the contralateral motor cortex of exp. 72-451 (at the level of section 3 in Fig. 1). The nomenclature of the bands is the same as m Fig. 1. low grain density, often background, however, the labelling depended both on its own width and the grain density of the neighbouring bands. Bands and interspaces could be followed from one section to the other (150/~m apart), while grain density and width of band and interspace varied with increasing distance. Similar bands were also observed on the ipsilateral side around the injection field and its immediate vicinity inspite of the high labelling. A p a r t from a higher grain density ipsilaterally, the arrangement of bands and interspaces was comparable to those on the contralateral side; however, to prove that they were the mirror image

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Fig. 3. A two-dimensional reconstruction of the pattern of grain density over the contralateral cortex of exp. 72-451. The isodensity contours were reconstructed from 14 parallel frontal sections (details see text), and reveal a series of high and low grain (axon terminal) density zones running rostrocaudally (a more detailed analysis, however, may reveal a further subdivision in their anterior-posterior plane). The nomenclature of the zones on the right corresponds to the bands b-n in Figs. 1 and 2. The inset, left, indicates the orientation of the contour map on the contralateral cortex (R).

needs a m o r e detailed analysis. N u m e r o u s sets o f b a n d s a n d interspaces were also seen in the p r e c e n t r a l m o t o r a r e a a n d in the a d j a c e n t cingular cortex when extensive injections covered either the ' t r u n k ' o r ' a r m ' regions (exp. 72-449 a n d 72-450). I n addition, characteristic sets were present in exp. 73-319, after a restricted injection into the 'leg-tail' m o t o r cortex, b u t they were less n u m e r o u s a n d n a r r o w e r . In the cases where label was injected into the 'face' a n d 'finger' regions (exp. 72-448, 73-320 a n d 73-475) the b a n d s were scarcely visible in either hemisphere even with extensive injections. F r o m the p o s t c e n t r a l cortex a n d p a r t i c u l a r l y the rostral p o r t i o n o f the gyrus postcentralis we h a d the i m p r e s s i o n t h a t there were h o r i z o n t a l r a t h e r t h a n vertical bands. These lay p r e d o m i n a n t l y in layers I a n d VI, less in III. M o r e c a u d a l l y (areas

369 1, 2 and probably 5) the horizontal bands were broken up but never achieved the striking pattern of vertically oriented bands seen in the precentral area. The terms 'horizontal and vertical bands' on the other hand may be misleading, it may be better to speak of homogeneous (rostral postcentral cortex) and heterogeneous (precentral cortex) grain arrangements. To analyze the precentral arrangement of bands and interspaces more detailed, 14 serial sections (approx. 600 #m apart) were selected from the contralateral region indicated in Fig. 3. Detailed drawings of the silver grain pattern on each section were made using first a projector and then a microscope. The intensity of the labelling was classified into 5 categories on a subjective scale. The digitalized density ratings were then transcribed onto a straight line using landmarks such as points I-IV in Fig. 3 to align the sections. Contours of isograin-density were then drawn between similar categories from one section to the other over the surface of the cortex. In trying to combine subdivisions of similar density from section to section and in an attempt to plot a comprehensive map of the course of the bands across the cortex, we reduced the original 5 density categories to 4. By drawing such subjective 'isodensity' curves it appeared that we were dealing with zones of low and high density rather than of bands and interspaces. There seems to be indeed rostrocaudally directed band-like zones which may split and coalesce in a similar manner to those described in the visual cortex 5. The density of these zones, however, varies in the rostrocaudal plane (Fig. 3, band b, c and n), as well as in mediolateral direction (band d) and this pattern becomes more and more irregular (band f-m) as one approaches the region homotopic to the injection site. The bands f-m are mostly well demarcated but the interpretation of 'bands' as something essentially different from an 'interspace' seems questionable in this region since the grain density in the 'interspace' was positive, although perhaps overestimated (due to a breakdown and spread of radioactive material from highly labelled terminals into adjacent regions) and it may be a zone in its own right rather than a negative interspace. These are preliminary results. The zones are not directly comparable with the physiological data suggesting a mosaic or overlapping organization of pyramidal cells projecting to spinal motoneurons. There is, however, a certain similarity between zones of high and low axon terminal density with the colonies of highest (best point) and minimal texture (cell density within a colony) 1,9, optimal and total projection areas 6, as well as with sharply defined or overlapping efferent zones 8. They all indicate that beside a somatotopic and laminar precentral cortical organization there is a vertically oriented system where intrinsic and extrinsic fibres may be quite selectively arranged. Further anatomical and physiological investigations are certainly worth continuing. The author thanks Prof. K. Akert for his help throughout the course of the experiment and Prof. J. M. van Buren and Dr. J. Bi~ttner for reading the manuscript. The technical assistance of R. Emch, A. FEh, J. B. Frei, H. Hauser. D. Savini and E. Schneider is gratefully acknowledged. Supported by grants from the Swiss National Foundation for Scientific Re-

370 s e a r c h N o s . 3.368.0.74 a n d 3.124.73 a n d t h e D r . Eric S l a c k - G y r F o u n d a t i o n , Z u r i c h .

1 ANDERSEN,P., HAGAN, P J , PHILLIPS,C G , AND POWELL,T P S., Mapping by mlcrostlmulat~on of overlapping projections from area 4 to motor umts of the baboon's hand, Proc. roy. Soc B, 188 0975) 31-60. 2 ASANUMA,H , FERNANDEZ, J , SCHEIBEL, M. E , AND SCHEIBEL, A B , Characteristics of projections from the nucleus ventralis lateralis to the motor cortex in the cats. an anatomical and physiological study, Exp Brain Res, 20 (1974) 315-330 3 ASANUMA,H , AND ROSEN, I , Topographical orgamzatlon of cortical efferent zones projecting to distal forelimb muscles in monkeys, Exp. Brain Res, 14 (1972) 243-256. 4 COLONNIER,M , The structural design of the neocortex In J. C ECCLES(Ed.), Brain and Consciou,s Experience, Springer, Berhn, 1966, pp 1-23. 5 HUBEL, D H., AND WIESEL, T N., Laminar and columnar dlstrlbut,on of geniculocortical fibers in the macaque monkey, J. comp Neurol., 146 (1972) 421-450 6 JANI