Amygdala interneuron subtypes control fear learning through disinhibition

Nature. 2014 May 22;509(7501):453-8. doi: 10.1038/nature13258. Epub 2014 May 11.


Learning is mediated by experience-dependent plasticity in neuronal circuits. Activity in neuronal circuits is tightly regulated by different subtypes of inhibitory interneurons, yet their role in learning is poorly understood. Using a combination of in vivo single-unit recordings and optogenetic manipulations, we show that in the mouse basolateral amygdala, interneurons expressing parvalbumin (PV) and somatostatin (SOM) bidirectionally control the acquisition of fear conditioning--a simple form of associative learning--through two distinct disinhibitory mechanisms. During an auditory cue, PV(+) interneurons are excited and indirectly disinhibit the dendrites of basolateral amygdala principal neurons via SOM(+) interneurons, thereby enhancing auditory responses and promoting cue-shock associations. During an aversive footshock, however, both PV(+) and SOM(+) interneurons are inhibited, which boosts postsynaptic footshock responses and gates learning. These results demonstrate that associative learning is dynamically regulated by the stimulus-specific activation of distinct disinhibitory microcircuits through precise interactions between different subtypes of local interneurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala / cytology*
  • Amygdala / physiology*
  • Animals
  • Conditioning, Classical
  • Electroshock
  • Fear / physiology*
  • Hindlimb
  • Inhibition, Psychological*
  • Interneurons / metabolism*
  • Learning / physiology*
  • Male
  • Mice
  • Optogenetics
  • Parvalbumins / metabolism
  • Somatostatin / metabolism
  • Synapses / metabolism


  • Parvalbumins
  • Somatostatin