Feedback in the brainstem: an excitatory disynaptic pathway for control of whisking

J Comp Neurol. 2015 Apr 15;523(6):921-42. doi: 10.1002/cne.23724. Epub 2015 Jan 30.

Abstract

Sensorimotor processing relies on hierarchical neuronal circuits to mediate sensory-driven behaviors. In the mouse vibrissa system, trigeminal brainstem circuits are thought to mediate the first stage of vibrissa scanning control via sensory feedback that provides reflexive protraction in response to stimulation. However, these circuits are not well defined. Here we describe a complete disynaptic sensory receptor-to-muscle circuit for positive feedback in vibrissa movement. We identified a novel region of trigeminal brainstem, spinal trigeminal nucleus pars muralis, which contains a class of vGluT2+ excitatory projection neurons involved in vibrissa motor control. Complementary single- and dual-labeling with traditional and virus tracers demonstrate that these neurons both receive primary inputs from vibrissa sensory afferent fibers and send monosynaptic connections to facial nucleus motoneurons that directly innervate vibrissa musculature. These anatomical results suggest a general role of disynaptic architecture in fast positive feedback for motor output that drives active sensation.

Keywords: AB_10003058; AB_10013220; AB_10563390; AB_2336126; AB_303884; AB_90738; active sensing; reflex; spinal nuclei; trigeminus; vibrissa; viral tracers.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways / physiology*
  • Animals
  • Brain Stem / cytology*
  • Brain Stem / physiology
  • Cholera Toxin / metabolism
  • Choline O-Acetyltransferase / genetics
  • Choline O-Acetyltransferase / metabolism
  • Feedback, Sensory / physiology*
  • Glutamate Decarboxylase / genetics
  • Glutamate Decarboxylase / metabolism
  • Glycine Plasma Membrane Transport Proteins / genetics
  • Glycine Plasma Membrane Transport Proteins / metabolism
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurons / physiology*
  • Reflex / physiology
  • Spinal Cord / cytology
  • Spinal Cord / physiology
  • Synapses / physiology*
  • Vagus Nerve / physiology
  • Vesicular Glutamate Transport Protein 2 / genetics
  • Vesicular Glutamate Transport Protein 2 / metabolism
  • Vesicular Inhibitory Amino Acid Transport Proteins / genetics
  • Vesicular Inhibitory Amino Acid Transport Proteins / metabolism
  • Vibrissae / innervation*
  • Vibrissae / metabolism

Substances

  • Glycine Plasma Membrane Transport Proteins
  • Luminescent Proteins
  • Slc17a6 protein, mouse
  • Vesicular Glutamate Transport Protein 2
  • Vesicular Inhibitory Amino Acid Transport Proteins
  • Viaat protein, mouse
  • Cholera Toxin
  • Choline O-Acetyltransferase
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1