Literature DB >> 24814341

Amygdala interneuron subtypes control fear learning through disinhibition.

Steffen B E Wolff1, Jan Gründemann2, Philip Tovote3, Sabine Krabbe3, Gilad A Jacobson3, Christian Müller3, Cyril Herry4, Ingrid Ehrlich5, Rainer W Friedrich3, Johannes J Letzkus6, Andreas Lüthi2.   

Abstract

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.

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Year:  2014        PMID: 24814341     DOI: 10.1038/nature13258

Source DB:  PubMed          Journal:  Nature        ISSN: 0028-0836            Impact factor:   49.962


  57 in total

1.  Regulation of neuronal input transformations by tunable dendritic inhibition.

Authors:  Matthew Lovett-Barron; Gergely F Turi; Patrick Kaifosh; Peter H Lee; Frédéric Bolze; Xiao-Hua Sun; Jean-François Nicoud; Boris V Zemelman; Scott M Sternson; Attila Losonczy
Journal:  Nat Neurosci       Date:  2012-01-15       Impact factor: 24.884

2.  Dendritic calcium spikes induce bi-directional synaptic plasticity in the lateral amygdala.

Authors:  Yann Humeau; Andreas Lüthi
Journal:  Neuropharmacology       Date:  2006-08-04       Impact factor: 5.250

3.  Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons.

Authors:  Alan R Woodruff; Pankaj Sah
Journal:  J Neurophysiol       Date:  2007-08-22       Impact factor: 2.714

4.  Switching on and off fear by distinct neuronal circuits.

Authors:  Cyril Herry; Stephane Ciocchi; Verena Senn; Lynda Demmou; Christian Müller; Andreas Lüthi
Journal:  Nature       Date:  2008-07-09       Impact factor: 49.962

Review 5.  Cortical pathways to the mammalian amygdala.

Authors:  A J McDonald
Journal:  Prog Neurobiol       Date:  1998-06       Impact factor: 11.685

6.  Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala.

Authors:  W Woodson; C R Farb; J E Ledoux
Journal:  Synapse       Date:  2000-11       Impact factor: 2.562

7.  Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of Calbindin-D(28k).

Authors:  A J McDonald; R L Betette
Journal:  Neuroscience       Date:  2001       Impact factor: 3.590

Review 8.  Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations.

Authors:  Thomas Klausberger; Peter Somogyi
Journal:  Science       Date:  2008-07-04       Impact factor: 47.728

9.  Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat.

Authors:  A J McDonald
Journal:  J Comp Neurol       Date:  1984-02-01       Impact factor: 3.215

10.  CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala.

Authors:  Yu Zhou; Jaejoon Won; Mikael Guzman Karlsson; Miou Zhou; Thomas Rogerson; Jayaprakash Balaji; Rachael Neve; Panayiota Poirazi; Alcino J Silva
Journal:  Nat Neurosci       Date:  2009-09-27       Impact factor: 24.884

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  194 in total

Review 1.  Information processing in the CNS: a supramolecular chemistry?

Authors:  Arturo Tozzi
Journal:  Cogn Neurodyn       Date:  2015-03-10       Impact factor: 5.082

Review 2.  Manipulating neural activity in physiologically classified neurons: triumphs and challenges.

Authors:  Felicity Gore; Edmund C Schwartz; C Daniel Salzman
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-19       Impact factor: 6.237

Review 3.  Contemporary approaches to neural circuit manipulation and mapping: focus on reward and addiction.

Authors:  Benjamin T Saunders; Jocelyn M Richard; Patricia H Janak
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-19       Impact factor: 6.237

Review 4.  Architectural Representation of Valence in the Limbic System.

Authors:  Praneeth Namburi; Ream Al-Hasani; Gwendolyn G Calhoon; Michael R Bruchas; Kay M Tye
Journal:  Neuropsychopharmacology       Date:  2015-12-09       Impact factor: 7.853

Review 5.  Optogenetic investigation of neural mechanisms for alcohol-use disorder.

Authors:  Barbara Juarez; Yutong Liu; Lu Zhang; Ming-Hu Han
Journal:  Alcohol       Date:  2018-06-19       Impact factor: 2.405

Review 6.  Synaptic encoding of fear memories in the amygdala.

Authors:  Reed L Ressler; Stephen Maren
Journal:  Curr Opin Neurobiol       Date:  2018-09-11       Impact factor: 6.627

7.  Sex- and Estrus-Dependent Differences in Rat Basolateral Amygdala.

Authors:  Shannon R Blume; Mari Freedberg; Jaime E Vantrease; Ronny Chan; Mallika Padival; Matthew J Record; M Regina DeJoseph; Janice H Urban; J Amiel Rosenkranz
Journal:  J Neurosci       Date:  2017-09-27       Impact factor: 6.167

8.  Cortical Synaptic Inhibition Declines during Auditory Learning.

Authors:  Emma C Sarro; Gardiner von Trapp; Todd M Mowery; Vibhakar C Kotak; Dan H Sanes
Journal:  J Neurosci       Date:  2015-04-22       Impact factor: 6.167

9.  Associative and plastic thalamic signaling to the lateral amygdala controls fear behavior.

Authors:  Boglárka Barsy; Kinga Kocsis; Aletta Magyar; Ákos Babiczky; Mónika Szabó; Judit M Veres; Dániel Hillier; István Ulbert; Ofer Yizhar; Ferenc Mátyás
Journal:  Nat Neurosci       Date:  2020-04-13       Impact factor: 24.884

Review 10.  An Emerging Circuit Pharmacology of GABAA Receptors.

Authors:  Elif Engin; Rebecca S Benham; Uwe Rudolph
Journal:  Trends Pharmacol Sci       Date:  2018-06-11       Impact factor: 14.819

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