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Long-Range Connectivity Defines Behavioral Specificity of Amygdala Neurons

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Senn, Verena, Wolff, Steffen B.E., Herry, Cyril, Grenier, François, Ehrlich, Ingrid, Gründemann, Jan, Fadok, Jonathan P., Müller, Christian, Letzkus, Johannes J., Lüthi, Andreas·2014·Neuron

DOI 10.1016/j.neuron.2013.11.006

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Abstract

Memories are acquired and encoded within large-scale neuronal networks spanning different brain areas. The anatomical and functional specificity of such long-range interactions and their role in learning is poorly understood. The amygdala and the medial prefrontal cortex (mPFC) are interconnected brain structures involved in the extinction of conditioned fear. Here, we show that a defined subpopulation of basal amygdala (BA) projection neurons targeting the prelimbic (PL) subdivision of mPFC is active during states of high fear, whereas BA neurons targeting the infralimbic (IL) subdivision are recruited, and exhibit cell-type-specific plasticity, during fear extinction. Pathway-specific optogenetic manipulations demonstrate that the activity balance between pathways is causally involved in fear extinction. Together, our findings demonstrate that, although intermingled locally, long-range connectivity defines distinct subpopulations of amygdala projection neurons and indicate that the formation of long-term extinction memories depends on the balance of activity between two defined amygdala-prefrontal pathways.

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Authors: Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., Fadok, J. P., Müller, C., Letzkus, J. J., & Lüthi, A.
Affiliations: University of Basel (CH)
Friedrich Miescher Institute (CH)
Corresponding author: Lüthi, Andreas
ORCID: Wolff, Steffen B.E.
Herry, Cyril
Ehrlich, Ingrid
Gründemann, Jan
Fadok, Jonathan P.
Müller, Christian
Letzkus, Johannes J.
Lüthi, Andreas
Venue: Neuron
Publisher: Elsevier BV
Published: 2014-01
Volume: 81
Issue: 2
Pages: 428-437
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2013.11.006
OpenAlex: W1977502547
Cited by: 522
References: 38
Citations by year: 2026: 17 · 2025: 28 · 2024: 35 · 2023: 35 · 2022: 40 · 2021: 55 · 2020: 45 · 2019: 52 · 2018: 55 · 2017: 47 · 2016: 30 · 2015: 49 · 2014: 34
FWCI: 29.74
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 386 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: amygdala, medial prefrontal cortex, fear extinction, long-range connectivity, prelimbic cortex, infralimbic cortex, memory extinction, optogenetic manipulation, fear conditioning
MeSH terms: Channelrhodopsins, Acoustic Stimulation, Action Potentials, Amygdala, Analysis of Variance, Animals, Bacterial Proteins, Biophysics, Cell Count, Conditioning, Classical, Elapid Venoms, Electric Stimulation, Extinction, Psychological, Fear, Hippocampus, Light, Luminescent Proteins, Male, Neural Pathways, Neurons, Peptides, Time Factors, Oncogene Proteins v-fos, Prefrontal Cortex, Herpesvirus 1, Human, Patch-Clamp Techniques, Mice, Biophysical Phenomena, Optogenetics, In Vitro Techniques

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Long-Range Connectivity Defines Behavioral Specificity of Amygdala Neurons

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