Corticothalamic gating of population auditory thalamocortical transmission in mouse

Abstract

The mechanisms that govern thalamocortical transmission are poorly understood. Recent data have shown that sensory stimuli elicit activity in ensembles of cortical neurons that recapitulate stereotyped spontaneous activity patterns. Here, we elucidate a possible mechanism by which gating of patterned population cortical activity occurs. In this study, sensory-evoked all-or-none cortical population responses were observed in the mouse auditory cortex in vivo and similar stochastic cortical responses were observed in a colliculo-thalamocortical brain slice preparation. Cortical responses were associated with decreases in auditory thalamic synaptic inhibition and increases in thalamic synchrony. Silencing of corticothalamic neurons in layer 6 (but not layer 5) or the thalamic reticular nucleus linearized the cortical responses, suggesting that layer 6 corticothalamic feedback via the thalamic reticular nucleus was responsible for gating stochastic cortical population responses. These data implicate a corticothalamic-thalamic reticular nucleus circuit that modifies thalamic neuronal synchronization to recruit populations of cortical neurons for sensory representations.

Corticothalamic Pathways in Auditory Processing: Recent Advances and Insights From Other Sensory Systems

“…This reduction was due to short-term synaptic depression of the TRN-thalamus synapse, with a minimal contribution from the intrinsically mediated reductions in TRN spiking (the intrinsic burst properties of TRN neurons cannot follow high frequencies; Crandall et al, 2015 ). A recent study in the auditory system investigated the mechanisms underlying the gating of all-or-none population responses in the auditory cortex via L6 CT-TRN feedback (Ibrahim et al, 2021 ). They present an alternative mechanism by which the gating of cortical activity mediated by L6 CT-TRN feedback is dependent on the ability of the TRN to desynchronize thalamocortical neurons rather than diminishing thalamic activity (Ibrahim et al, 2021 ).…”

“…A recent study in the auditory system investigated the mechanisms underlying the gating of all-or-none population responses in the auditory cortex via L6 CT-TRN feedback (Ibrahim et al, 2021 ). They present an alternative mechanism by which the gating of cortical activity mediated by L6 CT-TRN feedback is dependent on the ability of the TRN to desynchronize thalamocortical neurons rather than diminishing thalamic activity (Ibrahim et al, 2021 ). They suggest that thalamic synchronization by the TRN can be a mechanism to recruit neuronal populations for sensory representations (Ibrahim et al, 2021 ).…”

“…Recent studies using a combination of layer or cell-type specific selective manipulation, electrophysiology and behavior testing have just started to unravel the roles of CT pathways in behavior and perception (Guo et al, 2017 ; Nakayama et al, 2018 ; Clayton et al, 2021 ; Ibrahim et al, 2021 ; Lohse et al, 2021 ). For example, Homma et al ( 2017 ) used chromophore-targeted laser photolysis to selectively eliminate the input from layer VI to the MGV.…”

“…Altogether, these different CT circuits enrich and diversify the opportunities for bidirectional communication between thalamus and cortex. At the thalamic node, CT circuits actively transform and/or gate the transmission of sensory information en route to the cortex (Yu et al, 2004 ; Antunes and Malmierca, 2011 ; Mease et al, 2014 ; Cai et al, 2016 ; Guo et al, 2017 ; Homma et al, 2017 ; Ibrahim et al, 2021 ) but also regulate functional connectivity within and across cortical areas (Saalmann et al, 2012 ; Sherman, 2016 ; Zhou et al, 2016 ; Schmitt et al, 2017 ; Jaramillo et al, 2019 ). CT circuits expand the computational capabilities of the thalamus, reflecting its active role in sensory processing and beyond (Nakajima and Halassa, 2017 ; Rikhye et al, 2018 ).…”

Lemniscal Corticothalamic Feedback in Auditory Scene Analysis

“…As anatomical and physiological studies have shown (see section “A1-MGBv Corticothalamic Pathway”; Guo et al, 2017 ), corticothalamic feedback modulates not only MGBv but also A1 and TRN. Furthermore, corticothalamic feedback via TRN inhibiting MGBv seems to determine whether A1 neurons respond to weak tones or not ( Ibrahim et al, 2021 ). Future investigations will need to explore the joint effects of the combined thalamocortical-corticothalamic-corticoreticular-intracortical loop.…”