J. Physiol. (Paris) 93 (1999) 271-284 © 1999 Editions scientifiques et médicales Elsevier SAS. All rights reserved Visual inter-hemispheric processing: Constraints and potentialities set by axonal morphology Jean-Christophe Houzel a * , Chantal Milleret b a Max Planck Institut fiir Hirnforschung, Deutschordenstr. 49, 60528 Frankfurt/Main, Germany b Laboratoire de Physiologic de la Perception et de l'Action, CNRS UMR9950, Collège de France, II,Place Marcelin-Berthelot, 75005 Paris, France (Received 5 January 1999; accepted 3 February 1999) Abstract - The largest bundle of axonal fibers in the entire mammalian brain, namely the corpus callosum, is the pathway through which almost half a billion neurons scattered over all neocortical areas can exert an influence on their contralateral targets. These fibers are thus crucial participants in the numerous cortical functions requiring collaborative processing of information across the hemispheres. One of such operations is to combine the two partial cortical maps of the visual field into a single, coherent representation. This paper reviews recent anatomical, computational and electrophysiological studies on callosal connectivity in the cat visual system. We analyzed the morphology of individual callosal axons linking primary visual cortices using three-dimensional light-microscopic techniques. While only a minority of callosal axons seem to perform a strict ‘point-to-point’ mapping between retinotopically corresponding sites in both hemispheres, many others have widespread arbors and terminate into a handful of distant, radially oriented tufts. Therefore, the firing of a single callosal neuron might influence several cortical columns within the opposite hemisphere. Computer simulation was then applied to investigate how the intricate geometry of these axons might shape the spatio-temporal distribution of trans.callosal inputs. Based on the linear relation between diameter and conduction velocity of myelinated fibers, the theoretical delays required for a single action potential to reach all presynaptic boutons of a given arbor were derived from the caliber, g-ratio and length of successive axonal segments. This analysis suggests that the architecture of callosal axons is, in principle, suitable to promote the synchronous activation of multiple targets located across distant columns in the opposite hemisphere. Finally, electrophysiological recordings performed in several laboratories have shown the existence of stimulus-dependent synchronization of visual responses across the two hemispheres. Possible implications of these findings are discussed in the context of temporal tagging of neuronal assemblies. © 1999 Éditions scientifiques et médicales Elsevier SAS axonal tree / corpus callosum / spike propagation / temporal coding / visual cortex 1. Introduction 1.1. Two brains for one body? Before investigating possible correlations between structure and function at the level of single axonal trees, let us briefly consider more generally how the macroscopic structure of organisms relates to their behavior and, in turn, to the structure of their brains. Despite the fascinating diversity of forms encountered in the animal kingdom, both sensory and motor organs of almost all species, at least all arthropods and vertebrates, come pairwise and are located on each side of their longitudinal axis. Only those organs involved in internal regulation fail to comply with this rule, suggesting that the symmetric layout applies * Correspondence and reprints, present address: Lab. Neuro- plasticidade, Dept. Anatomia, Centro de Ciências da Saúde, UFRJ, 21941-590 Rio de Janeiro, Brasil. E-mail: jchouzel@anato.ufrj.br Abbreviations: CVM, central vertical meridian of the visual field; 17/18, cortical region forming the transition between the cytoarchitectonically defined visual areas Al7 and Al8. manifestly to the apparatuses enabling organisms to relate with their environment. Indeed, our senses basically proceed by a balance between pairs of sensors, as our acts result from a dynamic equilibrium between pairs of effecters, and our decisions often follow judgments from contrasting points of view. If one considers, as modem cognitive neuroscience teaches us to do, that the organization of mental representations somehow reflects the structure of the brain, it is not surprising that our encephalon also comes in two halves. Yet, the essence of this biparti- tion remains far from being clear. From early on, neurology and neuropsychology indicated a marked dichotomy between a ‘dominant’ hemisphere, usually the left one in right-handers, committed to analytical, sequential, verbal, local, ra- tional or objective processing, and a ‘minor’ hemi- sphere concerned rather with operations requiring synthetic, global, spatial, more intuitive or affective abilities. Such a trend to conceive each hemisphere as an entity able to achieve a variety of perceptual or mnemonic tasks on its own was encouraged by famous observations in commissurotomized patients [6, 17,