Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex

The Royal Society - Tập 304 Số 1119 - Trang 199-253 - 1984
Jonathan C. Horton1
1Department of Neurobiology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 02115, U.S.A.

Tóm tắt

In normal macaque monkeys a histochemical stain for cytochrome oxidase activity revealed a striking pattern of regularly spaced patches in primary visual (striate, area 17, V1) cortex. The patches were most obvious in layers II and III, but also in layers I, IV b, V and VI; only in layers IV c and IV a were they absent. The patches were oval shaped, about 250 by 150 pm and aligned into rows spaced about 350 pm apart. Along each row a patch was located about every 550 pm; often patches in neighbouring rows were aligned, creating a square array. T heir density was about one patch per 0.2 mm 2 (550 by 350 pm) in opercular cortex. The patches were also labelled preferentially by stains for lactate dehydrogenase, succinate dehydrogenase, acetylcholinesterase (AChE), and myelin. In V2, a coarser pattern of broad parallel stripes labelled by cytochrome oxidase, lactate dehydrogenase, and AChE was present. The cytochrome oxidase patches were absent in non-prim ate species like the cat, mink, tree shrew, mouse, rat, rabbit, and ground squirrel. However, they were present in all prim ate species examined, including the rhesus, cynomolgus, owl, and squirrel monkey, baboon, bushbaby, and hum an. While more species should be tested, it appears that the patches are a cytoarchitectonic feature unique to prim ate visual cortex. In the owl monkey patches of anterogradely transported horseradish peroxidase (HRP) were found in layers IV c a , III, and II after injection of the tracer into the lateral geniculate nucleus (l.g.n.). They coincided exactly with the position of patches in adjacent sections processed for cytochrome oxidase. A similar result was obtained in the macaque, except that patches were not present in layer IV c a . These experiments established that the cytochrome oxidase patches receive a direct, patchy projection from the lateral geniculate body. However, retrogradely filled layer VI cells in the owl monkey bore no regular relation to the patches. In the macaque, the ‘honeycomb’ of geniculate terminals in layer IV a matched a similar honeycomb pattern of cytochrome oxidase staining. In the Nissl stain three sublayers in layer IV a were identified: the honeycomb was located in layer IV a p . In V2, in the owl monkey the parallel stripes of enhanced cytochrome oxidase activity received a direct projection from l.g.n. or pulvinar. In the macaque, after intraocular injection of [ 3 H]proline, the rows of patches in layers II and III lay in register with ocular dominance columns seen by transneuronal radioautography in layer IV c. In another macaque, one eye was removed and the cortex stained for cytochrome oxidase, AChE and Nissl substance after six months survival. In layer IV c light and dark bands corresponding to the ocular dominance columns were visible; surprisingly the dark cytochrome oxidase bands matched the light AChE and Nissl bands. The set of bands belonging to the missing eye was determined by examining cytochrome oxidase staining and proline radioautographs in another macaque that sustained severe eye injury by [ 3 H]proline injection. In striate cortex, bands of radioactive label from the injured eye matched ocular dominance columns appearing more lightly stained by cytochrome oxidase. In the macaque tested six months after enucleation, in every other row the cytochrome oxidase patches appeared pale and shrunken. These lighter rows fit into precise register with the lighter ocular dominance columns in layer IV c, confirming the correspondence between rows of patches and ocular dominance columns demonstrated by proline injection. AChE staining of patches was similarly affected by eye removal. The effect of visual deprivation upon cytochrome oxidase staining was tested in two monocularly sutured macaques. In the l.g.n. no effect was detected. In visual cortex wide light columns alternating with thin dark columns were observed in layer IV. In one m acaque the ocular dominance columns were labelled independently by H R P injection into a deprived l.g.n. lamina. The H R P labelled ocular dominance columns fit within the pale cytochrome oxidase columns; this establishes that monocular deprivation causes a relatively greater loss of enzyme activity in ocular dom inance columns belonging to the closed eye. However, there was also loss of cytochrome oxidase staining along the borders of the normal eye dominance columns, indicating that ocular dominance columns in layer IV are subdivided into core zones flanked by border strips that are susceptible to loss of cytochrome oxidase activity with suture of either eye. The core zones are the same width as the rows of cytochrome oxidase patches and correspond to the dark bands seen in Liesegang stains of normal macaque striate cortex. In two adult cats the effect of monocular lid suture at 28 d old was assessed: no effect upon cytochrome oxidase staining in l.g.n. or cortex was observed. The optic disc representation in visual cortex was studied by 2-deoxyglucose radioautography and cytochrome oxidase staining after eye removal or lid suture in m acaque monkeys. It appeared as a pale oval, 1.65 times longer than the optic disc, a distortion probably required to m aintain overall isotrophy in magnification factor. Patches were present in the disc representation although ocular dominance columns are absent: they appeared rounder and more widely separated. In the temporal cresent patches were also present. They were larger, rounder, and less densely spaced than patches in binocular cortex. Deoxyglucose mapping in a macaque monkey monocularly stimulated with a display of parallel black and white stripes of irregular width and spacing rotated through all orientations has resulted in patches in the upper layers over ocular dominance columns corresponding to the open eye. These patches match cytochrome oxidase patches situated in every other row, thus suggesting that cells located in cytochrome oxidase patches respond to all orientations of stimulus. Macaques binocularly stimulated with vertical or horizontal stripes show a complicated pattern of deoxyglucose uptake, overlapping extensively with the pattern of cytochrome oxidase patches. In one monkey the right eye was removed and 18 d later the animal was stimulated with vertical stripes. Deoxyglucose radioautography and cytochrome oxidase staining combined in single tissue sections each revealed a matching pattern of ocular dominance columns in layer IV. In the upper layers, dots of radioautographic label were present, matching cytochrome oxidase patches in alternate rows. In foetal monkeys at E142-144 the laminar pattern of cytochrome oxidase staining in visual cortex was remarkable for a prominent wide band of intense activity in layer IV b and upper IV c a , absent in mature macaques. In tangential section, patches were visible in layers II, III and in layer IV b -IV c a , which indicates that patches form in monkey visual cortex before birth. The functional significance of the patches remains uncertain. It has been suggested that the visual field is analysed in visual cortex by small modules containing several hypercolumns of each stimulus variable. The cytochrome oxidase patches may constitute the anatomical correlate of these proposed modules.

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The Royal Society

Tập 304 Số 1119

199-253

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