Mechanisms underlying a thalamocortical transformation during active tactile sensation

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

    Research output: Contribution to journalArticlepeer-review

    13 Citations (Scopus)

    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.

    Original languageEnglish
    Article numbere1005576
    Number of pages31
    JournalPLOS Computational Biology
    Volume13
    Issue number6
    DOIs
    Publication statusPublished - Jun 2017

    Keywords

    • thalamocortical transformation
    • active tactile sensation
    • somatosensation
    • neural signals
    • tactile suppression
    • VPM neurons
    • thalamocortical circuit

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