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The neural basis of defensive behaviour evolution in Peromyscus mice

Evading imminent predator threat is critical for survival. Effective defensive strategies can vary, even between closely related species. However, the neural basis of such species-specific behaviours is still poorly understood. Here we find that two sister species of deer mice (genus Peromyscus) sho...

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Autores principales: Baier, Felix, Reinhard, Katja, Tong, Victoria, Murmann, Julie, Farrow, Karl, Hoekstra, Hopi E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10350006/
https://www.ncbi.nlm.nih.gov/pubmed/37461474
http://dx.doi.org/10.1101/2023.07.04.547734
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author Baier, Felix
Reinhard, Katja
Tong, Victoria
Murmann, Julie
Farrow, Karl
Hoekstra, Hopi E.
author_facet Baier, Felix
Reinhard, Katja
Tong, Victoria
Murmann, Julie
Farrow, Karl
Hoekstra, Hopi E.
author_sort Baier, Felix
collection PubMed
description Evading imminent predator threat is critical for survival. Effective defensive strategies can vary, even between closely related species. However, the neural basis of such species-specific behaviours is still poorly understood. Here we find that two sister species of deer mice (genus Peromyscus) show different responses to the same looming stimulus: P. maniculatus, which occupy densely vegetated habitats, predominantly dart to escape, while the open field specialist, P. polionotus, pause their movement. This difference arises from species-specific escape thresholds, is largely context-independent, and can be triggered by both visual and auditory threat stimuli. Using immunohistochemistry and electrophysiological recordings, we find that although visual threat activates the superior colliculus in both species, the role of the dorsal periaqueductal gray (dPAG) in driving behaviour differs. While dPAG activity scales with running speed and involves both excitatory and inhibitory neurons in P. maniculatus, the dPAG is largely silent in P. polionotus, even when darting is triggered. Moreover, optogenetic activation of excitatory dPAG neurons reliably elicits darting behaviour in P. maniculatus but not P. polionotus. Together, we trace the evolution of species-specific escape thresholds to a central circuit node, downstream of peripheral sensory neurons, localizing an ecologically relevant behavioural difference to a specific region of the complex mammalian brain.
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spelling pubmed-103500062023-07-17 The neural basis of defensive behaviour evolution in Peromyscus mice Baier, Felix Reinhard, Katja Tong, Victoria Murmann, Julie Farrow, Karl Hoekstra, Hopi E. bioRxiv Article Evading imminent predator threat is critical for survival. Effective defensive strategies can vary, even between closely related species. However, the neural basis of such species-specific behaviours is still poorly understood. Here we find that two sister species of deer mice (genus Peromyscus) show different responses to the same looming stimulus: P. maniculatus, which occupy densely vegetated habitats, predominantly dart to escape, while the open field specialist, P. polionotus, pause their movement. This difference arises from species-specific escape thresholds, is largely context-independent, and can be triggered by both visual and auditory threat stimuli. Using immunohistochemistry and electrophysiological recordings, we find that although visual threat activates the superior colliculus in both species, the role of the dorsal periaqueductal gray (dPAG) in driving behaviour differs. While dPAG activity scales with running speed and involves both excitatory and inhibitory neurons in P. maniculatus, the dPAG is largely silent in P. polionotus, even when darting is triggered. Moreover, optogenetic activation of excitatory dPAG neurons reliably elicits darting behaviour in P. maniculatus but not P. polionotus. Together, we trace the evolution of species-specific escape thresholds to a central circuit node, downstream of peripheral sensory neurons, localizing an ecologically relevant behavioural difference to a specific region of the complex mammalian brain. Cold Spring Harbor Laboratory 2023-07-05 /pmc/articles/PMC10350006/ /pubmed/37461474 http://dx.doi.org/10.1101/2023.07.04.547734 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Baier, Felix
Reinhard, Katja
Tong, Victoria
Murmann, Julie
Farrow, Karl
Hoekstra, Hopi E.
The neural basis of defensive behaviour evolution in Peromyscus mice
title The neural basis of defensive behaviour evolution in Peromyscus mice
title_full The neural basis of defensive behaviour evolution in Peromyscus mice
title_fullStr The neural basis of defensive behaviour evolution in Peromyscus mice
title_full_unstemmed The neural basis of defensive behaviour evolution in Peromyscus mice
title_short The neural basis of defensive behaviour evolution in Peromyscus mice
title_sort neural basis of defensive behaviour evolution in peromyscus mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10350006/
https://www.ncbi.nlm.nih.gov/pubmed/37461474
http://dx.doi.org/10.1101/2023.07.04.547734
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