Is most of neural plasticity in the thalamus cortical?

Abstract

We now have 20 years or more of rapidly accumulating evidence that sensory-perceptual systems, especially at the cortical level, are highly plastic, even in mature mammals (1-3). Much of the evidence comes from deprivation studies where part of the sensory input to a system is removed and the deactivated neurons in the brain stem and cortex recover responsiveness to remaining inputs. The recoveries can be immediate, but they also can have slowly developing components. The rapid reorganizations generally are attributed to a rebalancing of excititory and inhibitory factors within a dynamically maintained system.For various reasons, the major research emphasis has been on reorganizations in cortical sensory representations. Evidence for subcortical plasticity has been much more limited, and it sometimes is questioned. Nicolelis and coworkers (4, 5) have provided some of the most convincing recent evidence for subcortical changes in the receptive fields of neurons in the somatosensory thalamus, and in this issue of the Proceedings they now provide results indicating that the rapid adjustments are partially mediated by feedback inputs from cortex (6). Thus, not only do changes in the sources of activation occur for neurons in the thalamus, but most surprisingly, many of the changes depend on the poorly understood network of feedback connections that descend rather than ascend the hierarchy of processing levels in the somatosensory system. Sensory-perceptual systems consist of subcortical nuclei and cortical areas that are connected in a complex manner, with enough serial components that it is possible to assign hierarchical levels to structures (7). One of the basic features of these systems is that nuclei and areas that project to structures at higher levels nearly always receive projections back from these targets. Connections between the thalamus and cortex and between cortical areas are, with few exceptions, reciprocal. Projections to a higher level are called feed-forward; those to a lower level are feedback. The functions of feed-forward connections are, by far, better understood. The general premise has been that transformations in response properties mediated by local circuits of neurons at one level are relayed for further processing by neurons at the next level. Thus, the response properties of neurons become increasingly complex at higher and higher levels. This simple formulation of sensory processing postulates no clear role for the ubiquitous feedback connections. In a like manner, the general assumption in plasticity experiments has been that changes that occur in the receptive field properties of neurons at one level of the system have been created at that level or have accumulated in relays of information from lower levels. The report of Krupa et al. (6) is important in that it demonstrates that much of the plasticity that is observed at the thalamic level depends on feedback connections from the cortex. This finding challenges us to consider sensory-perceptual systems in the full richness of their...

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“…Evidence that cortical feedback also controls thalamic plasticity in the somatosensory system has been found by Krupa, Ghazanfar, and Nicolelis (1999) and by Parker and Dostrovsky (1999). These findings are reviewed by Kaas (1999).…”

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“…Diffuse connectivity may be called on to reroute signals after injury such as stroke. For example, somatosensory stimuli from a specific sensory system are preferentially routed through the thalamus to primary and secondary sensory areas dedicated to that body part, but they can also exhibit widely divergent activation patterns (28,30,34,43,53). VSD imaging in mice revealed surprisingly widespread intracortical connectivity between related regions of the cortex, such as sensory and motor areas (7,21,27,28,30).…”

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“…Cortical feedback also controls thalamic plasticity in the somatosensory system (Krupa, Ghazanfar, and Nicolelis, 1999;Parker and Dostrovsky, 1999). See Kaas (1999) for a review.…”