Frequency-specific response facilitation of supra and infragranular barrel cortical neurons depends on NMDA receptor activation in rats

Neuroscience. 2014 Dec 5;281:178-94. doi: 10.1016/j.neuroscience.2014.09.057. Epub 2014 Oct 2.

Abstract

Sensory experience has a profound effect on neocortical neurons. Passive stimulation of whiskers or sensory deprivation from whiskers can induce long-lasting changes in neuronal responses or modify the receptive field in adult animals. We recorded barrel cortical neurons in urethane-anesthetized rats in layers 2/3 or 5/6 to determine if repetitive stimulation would induce long-lasting response facilitation. Air-puff stimulation (20-ms duration, 40 pulses at 0.5-8Hz) was applied to a single whisker. This repetitive stimulation increased tactile responses in layers 2/3 and 5/6 for 60min. Moreover, the functional coupling (coherence) between the sensory stimulus and the neural response also increased after the repetitive stimulation in neurons showing response facilitation. The long-lasting response facilitation was due to activation of N-methyl-d-aspartate (NMDA) receptors because it was reduced by APV ((2R)-amino-5-phosphonovaleric acid, (2R)-amino-5-phosphonopentanoate) and MK801 application. Inactivation of layer 2/3 also blocked response facilitation in layer 5/6, suggesting that layer 2/3 may be fundamental in this synaptic plasticity processes. Moreover, i.p. injection of eserine augmented the number of layer 2/3 neurons expressing long-lasting response facilitation; this effect was blocked by atropine, suggesting that muscarinic receptor activation favors the induction of the response facilitation. Our data indicate that physiologically repetitive stimulation of a single whisker at the frequency at which rats move their whiskers during exploration of the environment induces long-lasting response facilitation improving sensory processing.

Keywords: LTP; sensory plasticity; somatosensory system; thalamocortical network; wavelet coherence.

MeSH terms

  • Animals
  • Atropine / pharmacology
  • Cholinesterase Inhibitors / pharmacology
  • Dizocilpine Maleate / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Muscarinic Antagonists / pharmacology
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Physical Stimulation
  • Physostigmine / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Somatosensory Cortex / drug effects
  • Somatosensory Cortex / physiology*
  • Valine / analogs & derivatives
  • Valine / pharmacology
  • Vibrissae / physiology*

Substances

  • Cholinesterase Inhibitors
  • Excitatory Amino Acid Antagonists
  • Muscarinic Antagonists
  • Receptors, N-Methyl-D-Aspartate
  • Dizocilpine Maleate
  • 2-amino-5-phosphopentanoic acid
  • Atropine
  • Physostigmine
  • Valine