The Functional Upregulation of Piriform Cortex Is Associated with Cross-Modal Plasticity in Loss of Whisker Tactile Inputs

Abstract

BackgroundCross-modal plasticity is characterized as the hypersensitivity of remaining modalities after a sensory function is lost in rodents, which ensures their awareness to environmental changes. Cellular and molecular mechanisms underlying cross-modal sensory plasticity remain unclear. We aim to study the role of different types of neurons in cross-modal plasticity.Methodology/Principal FindingsIn addition to behavioral tasks in mice, whole-cell recordings at the excitatory and inhibitory neurons, and their two-photon imaging, were conducted in piriform cortex. We produced a mouse model of cross-modal sensory plasticity that olfactory function was upregulated by trimming whiskers to deprive their sensory inputs. In the meantime of olfactory hypersensitivity, pyramidal neurons and excitatory synapses were functionally upregulated, as well as GABAergic cells and inhibitory synapses were downregulated in piriform cortex from the mice of cross-modal sensory plasticity, compared with controls. A crosswire connection between barrel cortex and piriform cortex was established in cross-modal plasticity.Conclusion/SignificanceAn upregulation of pyramidal neurons and a downregulation of GABAergic neurons strengthen the activities of neuronal networks in piriform cortex, which may be responsible for olfactory hypersensitivity after a loss of whisker tactile input. This finding provides the clues for developing therapeutic strategies to promote sensory recovery and substitution.

Coordinated Plasticity between Barrel Cortical Glutamatergic and GABAergic Neurons during Associative Memory

“…This selection was based on the studies of cross-modal plasticity [40, 41]. We did not trim the short whiskers since whisker trimming elevated the excitability of the barrel cortex [39].…”

Associations of Unilateral Whisker and Olfactory Signals Induce Synapse Formation and Memory Cell Recruitment in Bilateral Barrel Cortices: Cellular Mechanism for Unilateral Training Toward Bilateral Memory

“…This selection was based on the studies of cross-modal plasticity (Ni et al, 2010; Ye et al, 2012). We did not trim the short whiskers since whisker trimming elevated the excitability of the barrel cortex (Zhang et al, 2013).…”

Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs

“…This coordinate change is also seen synaptic transmission and input structures, since excitatory synaptic events and dendritic spines increase in a loss of whisker inputs (Figures 3 and 5). The coordination in the neurons and synapses is critical for them to work in a common purpose, i.e., the increase of neuronal sensitivity to inputs boost the activity of neuronal networks for cross-modal sensory plasticity [41,42]. In addition, we observed the bidirectional change between processes and their spines in apical and basal dendrites (Figures 4 and 5).…”

“…On the other hand, the functions of GABAergic neurons and synapses as well as the processes of receiving synaptic inputs are downregulated (Figures 6 and 8). These changes elevate the activity levels of network neurons in the barrel cortices, which may prevent a loss of their functions due to idle whisker inputs and increase their sensitivity to sensory inputs, as well as be ready to attracting the innervations from other sensory cortices and/or peripheral nerves for the remained modalities during the cross-modal sensory plasticity [39-42]. …”

“…In addition to reducing the threshold to boost neuronal networks, this upregulated activity may maintain the sensitivity of pyramidal neurons to weak input, so that their functions are not lost. Moreover, their upregulated activities may attract the exogenous inputs to innervate the barrel cortices, such as from piriform cortex [42], for cross-modal sensory plasticity and rehabilitation. Upregulations in the frequency of excitatory synaptic events (Figure 3) and the sites of receiving synaptic inputs (Figures 4 and 5) grant the establishment of new excitatory innervations in the barrel cortices.…”