Abstract
Processing of tactile sensory information in rodents is critically dependent on the communication between the primary somatosensory cortex (S1) and higher-order integrative cortical areas. Here, we have simultaneously characterized single-unit activity and local field potential (LFP) dynamics in the S1, primary visual cortex (V1), anterior cingulate cortex (ACC), posterior parietal cortex (PPC), while freely moving rats performed an active tactile discrimination task. Simultaneous single unit recordings from all these cortical regions revealed statistically significant neuronal firing rate modulations during all task phases (anticipatory, discrimination, response, and reward). Meanwhile, phase analysis of pairwise LFP recordings revealed the occurrence of long-range synchronization across the sampled fronto-parieto-occipital cortical areas during tactile sampling. Causal analysis of the same pairwise recorded LFPs demonstrated the occurrence of complex dynamic interactions between cortical areas throughout the fronto-parietal-occipital loop. These interactions changed significantly between cortical regions as a function of frequencies (i.e. beta, theta and gamma) and according to the different phases of the behavioral task. Overall, these findings indicate that active tactile discrimination by rats is characterized by much more widespread and dynamic complex interactions within the fronto-parieto-occipital cortex than previously anticipated.
Highlights
It is commonly assumed that tactile sensory processing is transmitted from the periphery to the cortex through parallel feedforward pathways, which ran through well-defined neuronal aggregates, grouped into rows and arcs, in the brainstem, thalamus, and somatosensory cortex, which altogether generate a multi-level isomorphic representation of the whiskers of the snout of most rodents[1,2]
We simultaneously recorded electrical activity from cortical neurons distributed across the frontal-parietal-occipital loop while rats performed an active tactile discrimination task
Analysis of these concurrent cortical recordings revealed the occurrence of statistically significant neuronal firing rate modulations throughout the anterior cingulate cortex (ACC), posterior parietal cortex (PPC), V1 and S1, during multiple phases of the task
Summary
It is commonly assumed that tactile sensory processing is transmitted from the periphery to the cortex through parallel feedforward pathways, which ran through well-defined neuronal aggregates, grouped into rows and arcs, in the brainstem (barrelets), thalamus (barreloids), and somatosensory (barrel) cortex, which altogether generate a multi-level isomorphic representation of the whiskers of the snout of most rodents[1,2] According to this classic model, the primary somatosensory cortex (S1) is a specialized cortical area dedicated to the processing of somatic information only. We hypothesized that active tactile discrimination may be mediated by widespread and dynamically complex bidirectional communication between S1 and other cortical areas located in the frontal, parietal, and even the occipital cortex (e.g. primary visual cortex) According to this hypothesis, both so called lower and higher order cortical areas interact differently depending on the animal’s behavior and the different phases of a tactile discrimination task. Our results revealed the existence of frequency-specific, and dynamically complex cortical interactions taking place throughout the fronto-parieto-occipital circuit during active tactile discrimination by rats
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