Presynaptic serotonin 2A receptors modulate thalamocortical plasticity and associative learning

Proc Natl Acad Sci U S A. 2016 Mar 8;113(10):E1382-91. doi: 10.1073/pnas.1525586113. Epub 2016 Feb 22.

Abstract

Higher-level cognitive processes strongly depend on a complex interplay between mediodorsal thalamus nuclei and the prefrontal cortex (PFC). Alteration of thalamofrontal connectivity has been involved in cognitive deficits of schizophrenia. Prefrontal serotonin (5-HT)2A receptors play an essential role in cortical network activity, but the mechanism underlying their modulation of glutamatergic transmission and plasticity at thalamocortical synapses remains largely unexplored. Here, we show that 5-HT2A receptor activation enhances NMDA transmission and gates the induction of temporal-dependent plasticity mediated by NMDA receptors at thalamocortical synapses in acute PFC slices. Expressing 5-HT2A receptors in the mediodorsal thalamus (presynaptic site) of 5-HT2A receptor-deficient mice, but not in the PFC (postsynaptic site), using a viral gene-delivery approach, rescued the otherwise absent potentiation of NMDA transmission, induction of temporal plasticity, and deficit in associative memory. These results provide, to our knowledge, the first physiological evidence of a role of presynaptic 5-HT2A receptors located at thalamocortical synapses in the control of thalamofrontal connectivity and the associated cognitive functions.

Keywords: 5-HT2A receptors; presynaptic NMDA receptors; serotonin; temporal-dependent plasticity; thalamocortical synapse.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Association Learning / physiology*
  • Blotting, Western
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / physiology*
  • Electrophysiological Phenomena
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Fluorescence
  • Neuronal Plasticity / genetics
  • Neuronal Plasticity / physiology*
  • Prefrontal Cortex / metabolism
  • Prefrontal Cortex / physiology
  • Protein Kinase C / metabolism
  • Rats, Sprague-Dawley
  • Receptor, Serotonin, 5-HT2A / genetics
  • Receptor, Serotonin, 5-HT2A / metabolism
  • Receptor, Serotonin, 5-HT2A / physiology*
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Synapses / metabolism
  • Synapses / physiology
  • Synaptic Transmission / genetics
  • Synaptic Transmission / physiology
  • Thalamus / metabolism
  • Thalamus / physiology*
  • Type C Phospholipases / metabolism

Substances

  • Receptor, Serotonin, 5-HT2A
  • Receptors, N-Methyl-D-Aspartate
  • Protein Kinase C
  • Type C Phospholipases