Collicular circuits for flexible sensorimotor routing

Abstract

Historically, cognitive processing has been thought to rely on cortical areas such as prefrontal cortex (PFC), with the outputs of these areas modulating activity in lower, putatively simpler spatiomotor regions, such as the midbrain superior colliculus (SC). Using a rat task in which subjects switch rapidly between task contexts that demand changes in sensorimotor mappings, we report a surprising role for the SC in non-spatial cognitive processes. Before spatial response choices could be formed, neurons in SC encoded task context more strongly than neurons in PFC, and bilateral SC silencing impaired behavioral performance. Once spatial choices could begin to be formed, SC neurons encoded the choice faster than PFC, while bilateral SC silencing no longer impaired choices. A set of dynamical models of the SC replicates our findings. Our results challenge cortically-focused views of cognition, and suggest that ostensibly spatiomotor structures can play central roles in nonspatiomotor cognitive processes..

Cortical feedback loops bind distributed representations of working memory

“…Neural inactivation studies have reported varying degrees to which different areas of the neocortex are required during delayed decision-making tasks [37][38][39][40][41][42] . Using our two-task design, we were able to isolate the inactivation effects that were specific to visual working memory, and this revealed the contribution of multiple cortical areas (Fig.…”

“…The role of different brain regions in maintaining memory-related task variables has previously been examined by optogenetic inactivation experiments [37][38][39][40][41][42] . To assess which cortical areas were required for working memory and to distinguish between their sensory, mnemonic and motor functions, we transiently inactivated one of six different cortical areas during one of two epochs per trial by focal optogenetic stimulation of inhibitory neurons (see Methods).…”

A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement

“…Planned movements that are released by a contextual ''Go cue'' are faster and more precise than unplanned movements (Hanes and Schall, 1996;Rosenbaum, 1980;Shenoy et al, 2013;Duan et al, 2021). Planned movements are anticipated by slowly varying neuronal activity in multiple connected brain areas, including the motor cortex (MCx), non-sensory thalamus, and others (Tanji and Evarts, 1976;Tanaka, 2007;Shenoy et al, 2013;Guo et al, 2017Guo et al, , 2018Svoboda and Li, 2018).…”

“…The motor planning mode collapses (Funahashi et al, 1989;Shadlen and Newsome, 2001;Kaufman et al, 2016Kaufman et al, , 2014, and a new activity mode with multi-phasic dynamics emerges (Churchland et al, 2012). This movement-type-specific mode is preferentially represented in the descending MCx neurons that project to premotor neurons in the brainstem and spinal cord (Li et al, 2015;Economo et al, 2018;Duan et al, 2021) and presumably serves as part of a motor command to initiate a specific movement. Another activity mode after the Go cue consists of changes that are invariant to the movement type (condition-invariant signal; Kaufman et al, 2016), referred to here as ''Go cue direction'' (D go ) mode.…”

Multiregional neural pathway: from movement planning to initiation

“…The different patterns of neuronal population activity in the motor cortex, thalamus, brainstem, and spinal cord are related to motor planning and execution. 2 , 3 However, to understand how neuronal dynamics in the cortex trigger motor execution, it is essential to explore the mechanism underlying the transition between those different modes in response to contextual Go cues (Fig. 1 ).…”