Delayed maturation and migration of excitatory neurons in the juvenile mouse paralaminar amygdala

Pia J Alderman; David Saxon; Lucía I Torrijos-Saiz; Malaz Sharief; Chloe E Page; Jude K Baroudi; Sean W Biagiotti; Vladimir A Butyrkin; Anna Melamed; Chay T Kuo; Stefano Vicini; Jose M García-Verdugo; Vicente Herranz-Pérez; Joshua G Corbin; Shawn F Sorrells

doi:10.1016/j.neuron.2023.11.010

Delayed maturation and migration of excitatory neurons in the juvenile mouse paralaminar amygdala

Neuron. 2024 Feb 21;112(4):574-592.e10. doi: 10.1016/j.neuron.2023.11.010. Epub 2023 Dec 11.

Authors

Affiliations

¹ Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA.
² Center for Neuroscience Research, Children's Research Institute, Children's National Hospital, Washington, DC 20011, USA; Interdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20007, USA.
³ Laboratory of Comparative Neurobiology, Cavanilles Institute of Biodiversity and Comparative Neurobiology, University of Valencia, CIBERNED-ISCIII, Valencia 46980, Spain.
⁴ Center for Neuroscience Research, Children's Research Institute, Children's National Hospital, Washington, DC 20011, USA; Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD 20742, USA.
⁵ Department of Cell Biology, Duke University School of Medicine, Durham, NC 27710, USA.
⁶ Interdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20007, USA; Department of Pharmacology & Physiology, Georgetown University Medical Center, Washington, DC 20007, USA.
⁷ Laboratory of Comparative Neurobiology, Cavanilles Institute of Biodiversity and Comparative Neurobiology, University of Valencia, CIBERNED-ISCIII, Valencia 46980, Spain; Department of Cell Biology, Functional Biology and Physical Anthropology, University of Valencia, Burjassot 46100, Spain.
⁸ Center for Neuroscience Research, Children's Research Institute, Children's National Hospital, Washington, DC 20011, USA.
⁹ Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, PA 15260, USA. Electronic address: shawn.sorrells@pitt.edu.

PMID: 38086370
PMCID: PMC10922384 (available on 2025-02-21)
DOI: 10.1016/j.neuron.2023.11.010

Abstract

The human amygdala paralaminar nucleus (PL) contains many immature excitatory neurons that undergo prolonged maturation from birth to adulthood. We describe a previously unidentified homologous PL region in mice that contains immature excitatory neurons and has previously been considered part of the amygdala intercalated cell clusters or ventral endopiriform cortex. Mouse PL neurons are born embryonically, not from postnatal neurogenesis, despite a subset retaining immature molecular and morphological features in adults. During juvenile-adolescent ages (P21-P35), the majority of PL neurons undergo molecular, structural, and physiological maturation, and a subset of excitatory PL neurons migrate into the adjacent endopiriform cortex. Alongside these changes, PL neurons develop responses to aversive and appetitive olfactory stimuli. The presence of this homologous region in both humans and mice points to the significance of this conserved mechanism of neuronal maturation and migration during adolescence, a key time period for amygdala circuit maturation and related behavioral changes.

Keywords: adolescence; birthdating; cross-species; doublecortin; endopiriform; human; intercalated; neurogenesis; postnatal development; transcriptomics.

MeSH terms

Adolescent
Adult
Affect
Amygdala
Animals
Basolateral Nuclear Complex*
Humans
Mice
Neural Stem Cells*
Neurons

Abstract

MeSH terms

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