Thalamocortical interactions shape hierarchical neural variability during stimulus perception

Abstract

The brain is hierarchically organized to process sensory signals. But, to what extent do functional connections within and across areas shape this hierarchical order? We addressed this problem in the thalamocortical network, while monkeys judged the presence or absence of a vibrotactile stimulus. We quantified the variability by means of intrinsic timescales and Fano factor, and functional connectivity by means of a directionality measure in simultaneously recorded neurons sharing the same cutaneous receptive field from the somatosensory thalamus (VPL) and areas 3b and 1 from the somatosensory cortex. During the pre-stimulus periods, VPL and area 3b exhibited similarly fast dynamics while area 1 showed much slower timescales. Furthermore, during the stimulus presence, the Fano factor increased along the network VPL-3b-1. In parallel, VPL established two separate main feedforward pathways with areas 3b and 1 to process stimulus information. While feedforward interactions from VPL and area 3b were favored by neurons within specific Fano factor ranges, neural variability in area 1 was invariant to the incoming pathways. In contrast to VPL and area 3b, during the stimulus arrival, area 1 showed significant intra-area interactions, which mainly pointed to neurons with slow intrinsic timescales. Overall, our results suggest that the lower variability of VPL and area 3b regulates feedforward thalamocortical communication, while the higher variability of area 1 supports intra-cortical interactions during sensory processing. These results provide evidence of a hierarchical order along the thalamocortical network.