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Plasticity of Local-Circuit Constraint Properties During Functional Reorganization of Adult Cortex

  • Author(s): Paullus, Jeffrey Richard
  • Advisor(s): Hickmott, Peter W
  • et al.
Abstract

Cortical sensory maps are highly organized structures that contain point-to-point representations of sensory inputs. This organization emerges in-part from horizontal connections that limit activity-flow across representational borders (local-circuit constraint properties). Interestingly, this organization undergoes experience-dependent modifications throughout life. This dissertation examines changes in local-circuit constraint properties during cortical reorganization.

Synaptic plasticity of horizontal connections could modify activity-flow across borders. Very little is known about inhibitory synaptic plasticity, its relationship to excitatory synaptic plasticity, and their relationship to functional organization. To investigate this, we located the forepaw/lower jaw (FP/LJ) of the primary somatosensory cortex (SI) in vivo, and used whole cell-patch electrophysiology to record excitatory and inhibitory responses of horizontal connections in vitro. Connections that remained within the representation (continuous) and those that crossed from one representation to another (discontinuous) were both examined before and after tetanization, allowing us to examine differences associated with borders. Tetanic stimulation induced diverse forms of synaptic plasticity, with long-term potentiation (LTP) dominating for excitation and long-term depression dominating for inhibition. The border did not restrict this plasticity in either case. In contrast, tetanization elicited LTP of monosynaptic inhibitory responses in continuous, but not discontinuous connections. These results demonstrate that continuous and discontinuous horizontal connections are capable of diverse plasticity responses that could theoretically functionally reorganize the cortex.

Axon remodeling could also change activity-flow across borders. To investigate this, we examined axon remodeling during long-durations of reorganization. We located the FP/LJ border and then iontophoresed a retrograde axonal tracer near the border at different durations of forelimb-denervation or sham-denervation. In sham-denervated animals, neurons close to the border had axonal projections oriented away from the border (axonal bias). Forelimb denervation resulted in a sustained change in border location and a significant reduction in the axonal bias after 6 weeks of denervation, but not after 4 or 12 weeks. The change in axonal bias resulted from axon sprouting across the border at 6 weeks, followed by the retraction of those axons by 12 weeks. This suggests bidirectional axonal rearrangements are associated with relatively long-durations of reorganization. Thus, diverse synaptic and morphological plasticity mechanisms could contribute to functional reorganization.

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