An interdigitated columnar mosaic of cytochrome oxidase, zinc, and neurotransmitter-related molecules in cat and monkey visual cortex.

Abstract

There is considerable physiological evidence for the compartmentalization of mammalian visual cortex into functional columnar modules, representing features of visual information processing such as eye and orientation specificity.However, anatomical markers of visual cortical compartmentalization have been described only for primate visual cortex. In this report, we describe an interdigitated mosaic of four neuroactive molecules which demarcate two distinct columnar systems in the kitten visual cortex. Serotonin 1C receptors and synaptic zinc were found to demarcate columns within layer IV ofkitten visual cortex, which were interdigitated with a second, patchy system characterized by increased levels of cytochrome oxidase and acetylcholinesterase. In primate visual cortex, as well as in the kitten, synaptic zinc was periodically distributed in a manner precisely complementary to cytochrome oxidase. These findings provide an anatomical framework on which unifying hypotheses of the functional organization of columnar systems in mammalian visual cortex can be built.The columnar arrangement of functionally similar elements has long been considered to be a fundamental principle of neocortical organization (1,2). The demonstration that cytochrome oxidase-enriched blobs overlie eye-specific columns in primate visual cortex (3) has proven to be invaluable in providing an anatomical reference point from which theories regarding the functional compartmentalization of mammalian visual cortex have evolved (reviewed in ref. 4). Since this discovery, the distributions of several enzymes and other molecules associated with the functions of neurotransmitters have been shown to be either coincident with or complementary to cytochrome oxidase blobs in primate visual cortex (4). Unfortunately, cytochrome oxidase blobs were reported to be unique to primates (5, 6), leading to hypotheses which constrained functional relationships ofthese blobs to features of visual processing also unique to primates. Recent studies, however, indicate the presence of a periodic distribution of cytochrome oxidase in the visual cortex of carnivores (7-9), thus providing an anatomical basis for columnar compartments common to both orders.The columnar parcellation of visual cortex into eye-and orientation-specific domains emerges in development as a result of input-and activity-dependent interactions between cortical afferents and their postsynaptic targets (10)(11)(12). This functional organization can be effectively modified by visual experience during a discrete temporal window of development (13-15). We have recently reported (16,17) that several anatomical markers of neurotransmitter specific-systems are arranged in a columnar manner in layer IV of striate cortex of cats and might, therefore, participate in the formation and plasticity ofits functional organization (16,17). In this report, we describe the topographical distribution of several neuroThe publication costs of this article were defrayed in part by page charge payment. This articl...

Anatomical Demonstration of Ocular Dominance Columns in Striate Cortex of the Squirrel Monkey

“…In the cat, the relationship between the CO staining in the upper layers and the ocular dominance columns is unclear (Dyck and Cynader, 1993;Murphy et al, 1995;Boyd and Matsubara, 1996). In the squirrel monkey, we found no correspondence between the patches and the ocular dominance columns.…”

Columnar distribution of serotonin-dependent plasticity within kitten striate cortex

“…The distribution of serotonergic receptors in cat visual cortex also changes in an age-dependent, regional, and laminar-specific manner (3). The most striking and specific pattern of developmentally regulated expression is the distribution of 5-HT 2C receptors into patches that separate layer IV of area 17 into 5-HT 2C receptor-rich and receptor-poor zones (3,4). A relationship to plasticity is suggested by the findings that monocular enucleation or dark rearing imposed early in life prevents the appearance of the patches (5), whereas in vivo studies have shown that blockade of the 5-HT 2C receptor class affects visual cortical activity-dependent plasticity (6,11).…”

“…1 summarizes autoradiographic and histochemical studies showing that, during the critical period, the kitten visual cortex transiently expresses a number of neurochemical markers in a columnar fashion. This columnar, biochemical architecture consists of two sets of complementary columns: one set is enriched in 5-HT 2C and 5-HT 2A receptors along with synaptic zinc, whereas the other expresses increased levels of CO and acetylcholinesterase (3,4). Among over 30 neurotransmitter receptors that have been studied within the visual cortex (1,2), only the 5-HT receptors noted above have been found to concentrate into columns within the developing cortex.…”

“…pecific, transient, regional, laminar, and columnar changes in the distribution of neurotransmitter-specific afferents and receptors have been shown to occur during the critical period of increased visual cortex plasticity (1)(2)(3)(4). Fig.…”

Serotonergic control of developmental plasticity

“…To test this hypothesis, Kojic et al (7) took advantage of the fact that this 5HT receptor patch system is complementary to another system of patches: the cytochrome oxidase (CO) blobs in layer II͞III. The CO blobs in layer II͞II are in register with 5HT receptor-poor patches in layer I V, whereas interblobs are on top of 5HT receptor-rich patches (15). Post hoc patch identification revealed that 5HT promoted the induction of LTP in 5HT2C receptor-rich patches and LTD in the receptor-poor patches (7).…”