Cortical responses to touch reflect subcortical integration of LTMR signals

TY - JOUR

T1 - Cortical responses to touch reflect subcortical integration of LTMR signals

AU - Emanuel, Alan J

AU - Lehnert, Brendan P

AU - Panzeri, Stefano

AU - Harvey, Christopher D

AU - Ginty, David D

N1 - © 2021. The Author(s), under exclusive licence to Springer Nature Limited.

PY - 2021/12

Y1 - 2021/12

N2 - Current models to explain how signals emanating from cutaneous mechanoreceptors generate representations of touch are based on comparisons of the tactile responses of mechanoreceptor subtypes and neurons in somatosensory cortex1-8. Here we used mouse genetic manipulations to investigate the contributions of peripheral mechanoreceptor subtypes to cortical responses to touch. Cortical neurons exhibited remarkably homogeneous and transient responses to skin indentation that resembled rapidly adapting (RA) low-threshold mechanoreceptor (LTMR) responses. Concurrent disruption of signals from both Aβ RA-LTMRs and Aβ slowly adapting (SA)-LTMRs eliminated cortical responses to light indentation forces. However, disruption of either LTMR subtype alone caused opposite shifts in cortical sensitivity but otherwise largely unaltered tactile responses, indicating that both subtypes contribute to normal cortical responses. Selective optogenetic activation of single action potentials in Aβ RA-LTMRs or Aβ SA-LTMRs drove low-latency responses in most mechanically sensitive cortical neurons. Similarly, most somatosensory thalamic neurons were also driven by activation of Aβ RA-LTMRs or Aβ SA-LTMRs. These findings support a model in which signals from physiologically distinct mechanoreceptor subtypes are extensively integrated and transformed within the subcortical somatosensory system to generate cortical representations of touch.

AB - Current models to explain how signals emanating from cutaneous mechanoreceptors generate representations of touch are based on comparisons of the tactile responses of mechanoreceptor subtypes and neurons in somatosensory cortex1-8. Here we used mouse genetic manipulations to investigate the contributions of peripheral mechanoreceptor subtypes to cortical responses to touch. Cortical neurons exhibited remarkably homogeneous and transient responses to skin indentation that resembled rapidly adapting (RA) low-threshold mechanoreceptor (LTMR) responses. Concurrent disruption of signals from both Aβ RA-LTMRs and Aβ slowly adapting (SA)-LTMRs eliminated cortical responses to light indentation forces. However, disruption of either LTMR subtype alone caused opposite shifts in cortical sensitivity but otherwise largely unaltered tactile responses, indicating that both subtypes contribute to normal cortical responses. Selective optogenetic activation of single action potentials in Aβ RA-LTMRs or Aβ SA-LTMRs drove low-latency responses in most mechanically sensitive cortical neurons. Similarly, most somatosensory thalamic neurons were also driven by activation of Aβ RA-LTMRs or Aβ SA-LTMRs. These findings support a model in which signals from physiologically distinct mechanoreceptor subtypes are extensively integrated and transformed within the subcortical somatosensory system to generate cortical representations of touch.

U2 - 10.1038/s41586-021-04094-x

DO - 10.1038/s41586-021-04094-x

M3 - SCORING: Journal article

C2 - 34789880

VL - 600

SP - 680

EP - 685

JO - NATURE

JF - NATURE

SN - 0028-0836

IS - 7890

ER -