Callosal Axons and Their Development

giorgio m. innocenti and Raymond bressoud abstract Recently, the anterograde transport of biocytin, coupled with computerized three-dimensional reconstruction and analysis, has allowed a detailed description of the morphology of the terminal arbors of callosal axons interconnecting the visual areas of the cat. Callosal axons are specific in their topographical distribution both across areas and within each area. Furthermore, they distribute different numbers of boutons to their various target sites. On the basis of computer simulations the geometry of most callosal axons appears tailored to the task of activating their targets in precise synchrony. The latter aspect of the morphology of callosal axons may be important for generating assemblies of coactive neurons in the two hemispheres during visual perception. Callosal axons differentiate in stages, each characterized by a combination of target-aimed and exuberant growth. The latter is corrected by regressive events that eliminate large numbers of callosal axons, their branches, and synapses. Together, target-aimed and exuberant growth progressively restrict the arbors to their sites of termination. The role of vision in the development of callosal axons is documented by the finding that binocular deprivation of vision by suture of the eyelids decreases the number of juvenile callosal connections that are stabilized into adulthood and stunts the development of the individual arbors.

The corpus callosum interconnects mainly cortical neurons of the two cerebral hemispheres and is by far the largest fiber tract in the brain. It consists of about 23 million axons in the cat (Berbel and Innocenti, 1988) and about 56 million in the rhesus monkey (LaMantia and Rakic, 1990a).

Callosal connections are organized according to a number of specific rules, some of which have been known for several years.

First, in all species the majority of callosal axons originate from pyramidal neurons in layer III (Figure 1.1). The infragranular layers V and VI contribute axons to some callosal projections, particularly to feedback projections from higher to lower areas (reviewed in In-nocenti, 1986; Kennedy, Meissirel, and Dehay, 1991).

giorgio m. innocenti Division of Neuroanatomy and Brain Development, Department of Neuroscience, Karolinska In-stitutet, Stockholm, Sweden.

Raymond bressoud Institut de Biologie Cellulaire et Morphologie, Lausanne, Switzerland.

The available electrophysiological and neurochemical evidence unequivocally establishes that the vast majority of these axons establish excitatory synapses. However, some axons probably terminate on inhibitory neurons and therefore have an inhibitory action on their targets (reviewed in Innocenti, 1986; Payne, 1994; Conti and Manzoni, 1994). The existence of a few directly inhibitory callosal axons seems probable in the cat (Hughes and Peters, 1992).

Second, each cortical area is connected with the corresponding area (homotopic callosal connections) and with noncorresponding areas in the contralateral hemisphere (heterotopic callosal connections; see Figure 1.2).

Third, each area is callosally connected to its own characteristic set of other areas. For example, the 17/18 region of the cat is connected to the contralateral 17/18 region as well as to peristriate areas such as 19 and 21a, the suprasylvian visual areas (Segraves and Rosenquist, 1982), and, in addition, to the insular cortex and to the claustrum (unpublished). The connections are usually reciprocal, and in general, areas that are callosally connected are also connected intrahemispherically (Figure 1.3). This suggests that areas in opposite hemispheres might communicate through a number of alternative intrahemispheric and interhemispheric routes, which might become differentially active in different functional conditions.

Fourth, callosal connections are unevenly distributed across the cortical areas (Figure 1.4; reviewed in Innocenti, 1986; Kennedy et al., 1991). In the visual system, callosal connections are restricted near the border between areas 17 and 18. This region represents the vertical meridian of the visual field and, in the cat, up to 20 degrees of visual field along it (Payne, 1994). A similarly restricted distribution of callosal connections is found in the primary somatosensory areas, along the representation of the body midlines, although part of the forepaw representation is also callosally connected. In addition to what was mentioned above, a different density of callosally projecting neurons was found in regions of the primary visual and somatosensory areas representing different sectors of the sensory peripheries

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