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In the current investigation, the neurophysiological organization of the neocortex was examined in adult animals that were bilaterally enucleated very early in life, before the retino-geniculocortical pathway was established. Our results indicate that some aspects of development of cortical fields are not mediated by specific sensory inputs. However, the current study also demonstrates that peripheral innervation plays a large role in the organization of the neocortex, as cortical territories normally involved in visual processing are completely captured by the auditory and somatosensory system. Thus, a large degree of phenotypic variability in cortical organization can be accomplished solely by removing or modifying sensory inputs.bilateral enucleations ͉ electrophysiological recording ͉ development ͉ evolution U ntil recently, the notion that humans with a congenital loss of one sensory system become better at making discriminations with the remaining sensory systems was mostly anecdotal. However, studies in congenitally blind individuals indicate that there is a shorter detection time for auditory discrimination tasks (1) and that blind individuals process language faster than sighted individuals (2). Thus, there is a compensatory adaptation of the auditory system in the congenitally blind, presumably because of a reorganization of the neocortex. This hypothesis is supported by recent neuroimaging studies of blind individuals demonstrating that both auditory localization tasks (3) and Braille reading (4-6) activate regions of cortex normally involved in visual processing. Similar types of cross-modal plasticity also have been demonstrated in congenitally deaf individuals (7-9). These results indicate that the amount of cortex devoted to a particular sensory system, and possibly the number and organization of cortical areas, is determined in large part by peripheral innervation and activity patterns generated with use. Indeed, a number of studies in the adult mammalian neocortex have demonstrated that cortical maps of sensory receptor arrays (areas) can be contracted or expanded by loss of peripheral inputs, or by enhanced use (10-24), and that cross-modal plasticity is possible when the modifications in peripheral activity patterns occur early in life (25). Yet, the extent to which peripheral innervation at early developmental stages can sculpt the architecture and function of entire sensory systems is not known.The present investigation was prompted by two seemingly disparate observations related to this issue. First, developmental studies demonstrate that thalamocortical input is not required for the expression of molecules believed to be involved in some aspects of cortical field development (26,27). This suggests that cortical arealization, or the emergence of cortical fields in development, is mediated by intrinsic genetic mechanisms that can operate independent of activity from peripheral receptors. This notion is difficult to reconcile with observations from comparative studies which demonstrate that t...

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Retinal cells that respond selectively to light onset or offset are segregated into On and Off pathways. Here, we describe the development of cone bipolar cells whose axonal arbors at maturity synapse onto ganglion cell dendrites confined to On and Off strata of the inner plexiform layer (IPL). In particular, we sought to determine whether the formation of this segregated pattern is dependent on the presence of ganglion cells. Developing bipolar cells were visualized using an antibody against recoverin, the calcium binding protein that labels On and Off cone bipolar cells in the adult rat retina. Recoverin-positive cells were apparent in the ventricular zone on the day of birth [postnatal day 0 (P0)], before bipolar cells begin to migrate to the inner nuclear layer. Two distinct strata were first apparent in the IPL at P8, with the Off pathway maturing earlier than the On pathway. There was no indication of exuberant bipolar cell projections. Throughout development, there were also a small number of recoverin-positive cells of unknown origin in the ganglion cell layer. To assess whether the formation of On and Off cone bipolar cell projections is dependent on the presence of ganglion cells, these target neurons were eliminated by unilateral section of the optic nerve. This was done on the day of birth, resulting in a total loss of ganglion cells 5-6 d before bipolar cell axons innervate the IPL. In retinas with optic nerve sections, On and Off cone bipolar cells were present, albeit at a lower than normal density, and the axonal arbors of these interneurons were organized into two distinct strata. This indicates that ganglion cells are not essential for the formation of segregated On and Off bipolar cell inputs. These results lend support to the hypothesis that specific ingrowth patterns of bipolar cell terminal arbors could regulate the formation of stratified retinal ganglion cell dendrites.

Theories of both cortical field development and cortical evolution propose that thalamocortical projections play a critical role in the differentiation of cortical fields (; ). In the present study, we examined how changing the size of the immature neocortex before the establishment of thalamocortical connections affects the subsequent development and organization of the adult neocortex. This alteration in cortex is consistent with one of the most profound changes made to the mammalian neocortex throughout evolution: cortical size. Removing the caudal one-third to three-fourths of the cortical neuroepithelial sheet unilaterally at an early stage of development in marsupials resulted in normal spatial relationships between visual, somatosensory, and auditory cortical fields on the remaining cortical sheet. Injections of neuroanatomical tracers into the reduced cortex revealed in an altered distribution of thalamocortical axons; this alteration allowed the maintenance of their original anteroposterior distribution. These results demonstrate the capacity of the cortical neuroepithelium to accommodate different cortical fields at early stages of development, although the anteroposterior and mediolateral relationships between cortical fields appear to be invariant. The shifting of afferents and efferents with cortical reduction or expansion at very early stages of development may have occurred naturally in different lineages over time and may be sufficient to explain much of the phenotypic variation in cortical field number and organization in different mammals.