Immediate and simultaneous sensory reorganization at cortical and subcortical levels of the somatosensory system

Abstract

The occurrence of cortical plasticity during adulthood has been demonstrated using many experimental paradigms. Whether this phenomenon is generated exclusively by changes in intrinsic cortical circuitry, or whether it involves concomitant cortical and subcortical reorganization, remains controversial. Here, we addressed this issue by simultaneously recording the extracellular activity of up to 135 neurons in the primary somatosensory cortex, ventral posterior medial nucleus of the thalamus, and trigeminal brainstem complex of adult rats, before and after a reversible sensory deactivation was produced by subcutaneous injections of lidocaine. Following the onset of the deactivation, immediate and simultaneous sensory reorganization was observed at all levels of the somatosensory system. No statistical difference was observed when the overall spatial extent of the cortical (9.1 ؎ 1.2 whiskers, mean ؎ SE) and the thalamic (6.1 ؎ 1.6 whiskers) reorganization was compared. Likewise, no significant difference was found in the percentage of cortical (71.1 ؎ 5.2%) and thalamic (66.4 ؎ 10.7%) neurons exhibiting unmasked sensory responses. Although unmasked cortical responses occurred at significantly higher latencies (19.6 ؎ 0.3 ms, mean ؎ SE) than thalamic responses (13.1 ؎ 0.6 ms), variations in neuronal latency induced by the sensory deafferentation occurred as often in the thalamus as in the cortex. These data clearly demonstrate that peripheral sensory deafferentation triggers a system-wide reorganization, and strongly suggest that the spatiotemporal attributes of cortical plasticity are paralleled by subcortical reorganization.The occurrence of cortical plastic reorganization following peripheral sensory deafferentation in adult animals has been demonstrated in every mammalian species investigated (1-4). Because this phenomenon has been observed in both sensory and motor cortical areas (5, 6), the ability to undergo functional reorganization seems to be a general property of the entire adult neocortex. Nevertheless, the mechanisms underlying cortical reorganization in adult animals remains the focus of an intense debate. Thus, whereas corticocortical connections have been implicated in the genesis of this phenomenon (7,8), considerable experimental data also support the notion that reorganization at subcortical levels can contribute to the occurrence of cortical plasticity (9-14). Recently, a few studies carried out in the somatosensory (15, 16) and visual (17) systems have suggested that cortical plasticity may result exclusively from synaptic alterations in intrinsic cortical circuitry. These findings have rekindled the debate by arguing against any fundamental role for subcortical structures in the process of cortical reorganization.Part of the difficulty in unequivocally establishing the contribution of subcortical structures to cortical plasticity lies in the fact that the evidence for subcortical reorganization has been usually obtained independently, without simultaneous characterization of the presu...

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