Repetitive Sensory Stimulation Potentiates and Recruits Sensory-Evoked Cortical Population Activity
Year: 2024
Type: article
Abstract: ABSTRACT Sensory experience and learning are thought to be associated with plasticity of neocortical circuits. Repetitive sensory stimulation can induce long-term potentiation (LTP) of cortical excitatory synapses in anesthetized mice; however, it is unclear if these phenomena are associated with sustained changes in activity during wakefulness. Here we used time-lapse, calcium imaging of layer (L) 2/3 neurons in the primary somatosensory cortex (S1), in awake male mice, to assess the effects of a bout of rhythmic whisker stimulation (RWS) at a frequency by which rodents sample objects. We found that RWS induced a 1h-increase in whisker-evoked L2/3 neuronal activity. This was not observed for whiskers functionally connected to distant cortical columns. We also found that RWS altered whether individual neurons encoded subsequent stimulus representation by either being recruited or suppressed. Vasoactive intestinal-peptide-expressing (VIP) interneurons, which promote plasticity through disinhibition of pyramidal neurons, were found to exclusively elevate activity during RWS. These findings indicate that cortical neurons’ representation of sensory input can be modulated over hours through repetitive sensory stimulation, which may be gated by activation of disinhibitory circuits. SIGNIFICANCE STATEMENT Sensory experience and learning are thought to be associated with the plasticity of cortical synaptic circuits. Here, we tested how repeated sensory stimulation changes subsequent sensory-evoked responses, using the mouse somatosensory cortex as a model. This cortical area processes, among others, sensory information from the whiskers. We found that rhythmic whisker stimulation potentiated excitatory neuronal activity for an hour, and identified a disinhibitory interneuron-mediated mechanism that could gate this plasticity. This work increases our understanding of sensory learning and experience-dependent plasticity processes by demonstrating that cortical representations of sensory input are dynamic and are effectively modulated by repeated sensory stimulation.
Source: Journal of Neuroscience
Language: English
Subfield: Cellular and Molecular Neuroscience
Field: Neuroscience
Domain: Life Sciences
Open Access status: hybrid
Funders: National Science Foundation, Brain and Behavior Research Foundation, National Alliance for Research on Schizophrenia and Depression, UK Research and Innovation, International Foundation for Research in Paraplegia, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, Directorate for Biological Sciences, Biotechnology and Biological Sciences Research Council
Awards: Activity-dependent functional and structural plasticity in the somatosensory cortex in vivo, Cortical synaptic circuit mechanisms for perceptual function and learning, G4080574980, The role of paralemniscal circuits in cortical plasticity and perception, G6031189682, Immunopathogenesis of spontaneous models of SLE: genetic, cellular and molecular analysis, G6673774195, VIP interneuron-mediated disinhibition underlies cortical network plasticity & perceptual learning
OpenAlex ID: W4404134434