Amygdala interneuron subtypes control fear learning through disinhibition

Steffen B. E. Wolff, Jan Gründemann, Philip Tovote, Sabine Krabbe, Gilad A. Jacobson, Christian Müller, Cyril Herry, Ingrid Ehrlich, Rainer W. Friedrich, Johannes J. Letzkus, Andreas Lüthi
Nature. 2014-05-01; 509(7501): 453-458
DOI: 10.1038/nature13258

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

Amygdala interneuron subtypes control fear learning through disinhibition.

Wolff SB(1), Gründemann J(2), Tovote P(3), Krabbe S(3), Jacobson GA(3), Müller
C(3), Herry C(4), Ehrlich I(5), Friedrich RW(3), Letzkus JJ(6), Lüthi A(2).

Author information:
(1)1] Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66,
CH-4058 Basel, Switzerland [2] University of Basel, 4000 Basel, Switzerland [3].
(2)1] Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66,
CH-4058 Basel, Switzerland [2].
(3)Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66,
CH-4058 Basel, Switzerland.
(4)INSERM U862, Neurocentre Magendie, 146 rue Leo Saignat, 33077 Bordeaux,
France.
(5)Hertie Institute for Clinical Brain Research, 72076 Tübingen, Germany.
(6)1] Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66,
CH-4058 Basel, Switzerland [2] Max-Planck Institute for Brain Research, 60438
Frankfurt, Germany. [3].

Comment in
Curr Biol. 2014 Aug 4;24(15):R690-3.

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.

DOI: 10.1038/nature13258
PMID: 24814341 [Indexed for MEDLINE]


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