Beyond maps: a dynamic view of the somatosensory system.
Current theories on how tactile information is processed by the mammalian somatosensory system are based primarily on data obtained in studies in which the physiological properties of single neurons were characterized, one at a time, in behaving or anesthetized animals. Yet, the central nervous system relies on the concurrent activation of large populations of neurons to process the variety of sensory stimuli that contribute to normal tactile perception. The recent introduction of electrophysiological methods for chronic and simultaneous recordings of the extracellular activity of large numbers of single neurons per animal has allowed us to investigate, for the first time, how populations of neurons, located at multiple processing stages of the somatosensory system, interact following passive and active tactile stimulation. The rat trigeminal somatosensory system was used as a model for this investigation. Our results revealed the existence of highly dynamic and distributed representations of tactile information, not only in the somatosensory cortex, but also in the thalamus and even in the brainstem. In these structures, we identified broadly tuned neurons with multiwhisker receptive fields (RFs). In the thalamus, a large percentage of neurons exhibited shifts in the spatial domain of their RFs as a function of post-stimulus time. During these shifts, the center of the neuron's RF moved across the whisker pad from caudal to rostral whiskers, but not in the opposite direction, suggesting that these spatiotemporal RFs may encode directional information. Further studies revealed that somatosensory representations were maintained by dynamic interactions between multiple convergent afferents, since they could be altered in a matter of seconds by reversible sensory deprivations. Overall, these results suggest that the rat somatosensory system relies on both spatial and temporal interactions between populations of cortical and subcortical neurons to process multiple attributes of tactile stimuli.
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