Mechanisms underlying a thalamocortical transformation during active tactile sensation.

Diego Adrian Gutnisky,Minh-Son To,Samuel Andrew Hires,Karel Svoboda,Jianing Yu,Michael Ross Bale,David Golomb,Peter E Latham

doi:10.1371/journal.pcbi.1005576

Abstract

During active somatosensation, neural signals expected from movement of the sensors are suppressed in the cortex, whereas information related to touch is enhanced. This tactile suppression underlies low-noise encoding of relevant tactile features and the brain’s ability to make fine tactile discriminations. Layer (L) 4 excitatory neurons in the barrel cortex, the major target of the somatosensory thalamus (VPM), respond to touch, but have low spike rates and low sensitivity to the movement of whiskers. Most neurons in VPM respond to touch and also show an increase in spike rate with whisker movement. Therefore, signals related to self-movement are suppressed in L4. Fast-spiking (FS) interneurons in L4 show similar dynamics to VPM neurons. Stimulation of halorhodopsin in FS interneurons causes a reduction in FS neuron activity and an increase in L4 excitatory neuron activity. This decrease of activity of L4 FS neurons contradicts the "paradoxical effect" predicted in networks stabilized by inhibition and in strongly-coupled networks. To explain these observations, we constructed a model of the L4 circuit, with connectivity constrained by in vitro measurements. The model explores the various synaptic conductance strengths for which L4 FS neurons actively suppress baseline and movement-related activity in layer 4 excitatory neurons. Feedforward inhibition, in concert with recurrent intracortical circuitry, produces tactile suppression. Synaptic delays in feedforward inhibition allow transmission of temporally brief volleys of activity associated with touch. Our model provides a mechanistic explanation of a behavior-related computation implemented by the thalamocortical circuit.

Highlights

Thalamocortical circuits represent model systems for multi-area computations [1]
We study how information is transformed between connected brain areas: the thalamus, the gateway to the cortex, and layer 4 (L4) in cortex, which is the first station to process sensory input from the thalamus
Tactile suppression is an example of adaptive filtering [25, 26], which is critical for low-noise encoding of relevant sensory stimuli

Summary

Introduction

Thalamocortical circuits represent model systems for multi-area computations [1]. Sensory information enters the cortex through the thalamus. Transformations in thalamocortical circuits have mostly been studied in anesthetized animals with passive sensory stimuli [2,3,4,5,6,7,8] or with artificial whisking [9]. Movement of the sensors produces ‘reafferent’ signals, whereas interactions with the world generate ‘exafferent’ signals. Movement attenuates the transmission of certain sensory signals to the cortex [22,23,24]. Tactile suppression is an example of adaptive filtering [25, 26], which is critical for low-noise encoding of relevant sensory stimuli. We identify the mechanisms of adaptive filtering in the thalamocortical circuit of the mouse whisker system

Methods

Results

Discussion

Conclusion