Abstract
The auditory thalamus is the central nexus of bottom-up connections from the inferior colliculus and top-down connections from auditory cortical areas. While considerable efforts have been made to investigate feedforward processing of sounds in the auditory thalamus (medial geniculate body, MGB) of non-human primates, little is known about the role of corticofugal feedback in the MGB of awake non-human primates. Therefore, we developed a small, repositionable cooling probe to manipulate corticofugal feedback and studied neural responses in both auditory cortex and thalamus to sounds under conditions of normal and reduced cortical temperature. Cooling-induced increases in the width of extracellularly recorded spikes in auditory cortex were observed over the distance of several hundred micrometers away from the cooling probe. Cortical neurons displayed reduction in both spontaneous and stimulus driven firing rates with decreased cortical temperatures. In thalamus, cortical cooling led to increased spontaneous firing and either increased or decreased stimulus driven activity. Furthermore, response tuning to modulation frequencies of temporally modulated sounds and spatial tuning to sound source location could be altered (increased or decreased) by cortical cooling. Specifically, best modulation frequencies of individual MGB neurons could shift either toward higher or lower frequencies based on the vector strength or the firing rate. The tuning of MGB neurons for spatial location could both sharpen or widen. Elevation preference could shift toward higher or lower elevations and azimuth tuning could move toward ipsilateral or contralateral locations. Such bidirectional changes were observed in many parameters which suggests that the auditory thalamus acts as a filter that could be adjusted according to behaviorally driven signals from auditory cortex. Future work will have to delineate the circuit elements responsible for the observed effects.
Highlights
The thalamus is traditionally conceptualized as a gateway between upstream inputs from subcortical structures to cortical areas (Sherman and Guillery, 2006)
To assess the effects of cortical cooling on thalamic response properties we focused on two types of stimuli: in a subset of neurons we focused on processing of temporal modulations and hereto typically tested neurons with pure tones at various intensities to characterize both frequency and intensity tuning
Over time we studied the effects of cooling of different parts of field AI by successively opening new craniotomies while closing old craniotomies with bone wax and dental acrylic (Figure 2)
Summary
The thalamus is traditionally conceptualized as a gateway between upstream inputs from subcortical structures to cortical areas (Sherman and Guillery, 2006). The feedforward and feedback connections between cortex and thalamus form an intricate cortico-thalamo-cortical loop (Winer and Larue, 1987; Happel et al, 2014; Mukherjee et al, 2020) whose structure-function relationship is still poorly understood (Usrey and Sherman, 2019). Diverse functions have been proposed for corticothalamic feedback in the auditory system, including gating of thalamocortical transmission (Yu et al, 2004; Ibrahim et al, 2021), supporting thalamic plasticity during learning (He, 2003; Suga, 2020; Taylor et al, 2021), gain control of cortical input (Saldeitis et al, 2021) and switching dynamics of processing to favor detection or discrimination of stimuli (Guo et al, 2017). More generally, it is apparent that thalamic sensory processing results from the dynamic interplay of feedforward and feedback pathways (Alitto and Usrey, 2003)
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