Neurexin-neuroligin transsynaptic interaction mediates learning-related synaptic remodeling and long-term facilitation in aplysia

Neuron. 2011 May 12;70(3):468-81. doi: 10.1016/j.neuron.2011.03.020.

Abstract

Neurexin and neuroligin, which undergo heterophilic interactions with each other at the synapse, are mutated in some patients with autism spectrum disorder, a set of disorders characterized by deficits in social and emotional learning. We have explored the role of neurexin and neuroligin at sensory-to-motor neuron synapses of the gill-withdrawal reflex in Aplysia, which undergoes sensitization, a simple form of learned fear. We find that depleting neurexin in the presynaptic sensory neuron or neuroligin in the postsynaptic motor neuron abolishes both long-term facilitation and the associated presynaptic growth induced by repeated pulses of serotonin. Moreover, introduction into the motor neuron of the R451C mutation of neuroligin-3 linked to autism spectrum disorder blocks both intermediate-term and long-term facilitation. Our results suggest that activity-dependent regulation of the neurexin-neuroligin interaction may govern transsynaptic signaling required for the storage of long-term memory, including emotional memory that may be impaired in autism spectrum disorder.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Aplysia
  • Arginine / genetics
  • Cell Adhesion Molecules, Neuronal / genetics
  • Cell Adhesion Molecules, Neuronal / metabolism*
  • Cells, Cultured
  • Central Nervous System / cytology
  • Cloning, Molecular / methods
  • Cysteine / genetics
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Green Fluorescent Proteins / genetics
  • Humans
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Microinjections / methods
  • Molecular Sequence Data
  • Motor Neurons / drug effects
  • Motor Neurons / physiology*
  • Mutation / genetics
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Oligodeoxyribonucleotides, Antisense / pharmacology
  • Protein Binding / physiology
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / physiology*
  • Serotonin / pharmacology
  • Synapses / metabolism
  • Synapses / physiology

Substances

  • Cell Adhesion Molecules, Neuronal
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Nrxn1 protein, rat
  • Oligodeoxyribonucleotides, Antisense
  • Receptors, Cell Surface
  • neuroligin 3
  • Green Fluorescent Proteins
  • Serotonin
  • Arginine
  • Cysteine

Associated data

  • GENBANK/HM448446
  • GENBANK/HM461999