Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression.

Xiao-Lin Chou,Huizhong W Tao,Qi Fang,Linqing Yan,Wen Zhong,Li I Zhang,Jinxing Wei,Haifu Li,Bo Peng

doi:10.7554/elife.54157

Abstract

Lateral posterior nucleus (LP) of thalamus, the rodent homologue of primate pulvinar, projects extensively to sensory cortices. However, its functional role in sensory cortical processing remains largely unclear. Here, bidirectional activity modulations of LP or its projection to the primary auditory cortex (A1) in awake mice reveal that LP improves auditory processing in A1 supragranular-layer neurons by sharpening their receptive fields and frequency tuning, as well as increasing the signal-to-noise ratio (SNR). This is achieved through a subtractive-suppression mechanism, mediated largely by LP-to-A1 axons preferentially innervating specific inhibitory neurons in layer 1 and superficial layers. LP is strongly activated by specific sensory signals relayed from the superior colliculus (SC), contributing to the maintenance and enhancement of A1 processing in the presence of auditory background noise and threatening visual looming stimuli respectively. Thus, a multisensory bottom-up SC-pulvinar-A1 pathway plays a role in contextual and cross-modality modulation of auditory cortical processing.

Highlights

Thalamus is generally considered as a gate to the cerebral cortex
We found that lateral posterior nucleus (LP) activity improved auditory processing functions in A1 in that it helped to sharpen frequency tuning of A1 L2/3 pyramidal neurons and to enhance the signal-to-noise ratio (SNR) of their auditory responses, through subtractive suppression of their responses in analogous to a thresholding effect
Bidirectional modulation of frequency tuning and SNR in A1 L2/3 by LP activity

Summary

Introduction

First-order thalamic nuclei, such as the dorsal lateral geniculate nucleus (dLGN) and ventral medial geniculate body (MGBv), relay bottom-up sensory information to primary sensory cortices, visual and auditory, respectively (Kremkow and Alonso, 2018; Winer et al, 2005). They serve as the major driver of sensory responses in the cortex for each respective sensory modality (Guillery and Sherman, 2002; Halassa and Sherman, 2019). We found that LP, by receiving salient input from SC, could mediate the cross-modality modulation of A1 responses by visual looming stimuli

Results

Discussion

Materials and methods