Cargando…

Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system

Losing a fight against a conspecific male (social defeat) induces a period of suppressed aggressiveness and general behaviour, often with symptoms common to human psychiatric disorders. Agonistic experience is also discussed as a potential cause of consistent, behavioral differences between individu...

Descripción completa

Detalles Bibliográficos
Autores principales: Rose, Jacqueline, Rillich, Jan, Stevenson, Paul A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5598953/
https://www.ncbi.nlm.nih.gov/pubmed/28910319
http://dx.doi.org/10.1371/journal.pone.0184121
_version_ 1783264007003570176
author Rose, Jacqueline
Rillich, Jan
Stevenson, Paul A.
author_facet Rose, Jacqueline
Rillich, Jan
Stevenson, Paul A.
author_sort Rose, Jacqueline
collection PubMed
description Losing a fight against a conspecific male (social defeat) induces a period of suppressed aggressiveness and general behaviour, often with symptoms common to human psychiatric disorders. Agonistic experience is also discussed as a potential cause of consistent, behavioral differences between individuals (animal “personality”). In non-mammals, however, the impact of single agonistic encounters typically last only hours, but then again studies of repeated intermittent defeat (chronic social defeat) are seldom. We report the effect of chronic social defeat in adult male crickets (Gryllus bimaculatus), for which all known behavioral effects of defeat last only 3 h. Firstly, after 48 h social isolation, crickets that experienced 5 defeats at 24 h intervals against the same, weight-matched opponent exhibited suppressed aggressiveness lasting >24 h, which was still evident when the animals were matched against an unfamiliar opponent at the last trial. Secondly, this longer-term depression of aggression also occurred in 48 h isolated crickets that lost 6 fights at 1 h intervals against unfamiliar opponents at each trial. Thirdly, crickets isolated as larvae until adult maturity (>16 days) were significantly more aggressive, and less variable in their aggressiveness at their very first fight than 48 h isolates, and also significantly more resilient to the effects of chronic social defeat. We conclude that losing an aggressive encounter in crickets has a residual effect, lasting at least 24 h, that accumulates when repeated defeats are experienced, and leads to a prolonged depression of aggressive motivation in subordinates. Furthermore, our data indicate that social interactions between young adults and possibly larvae can have even longer, possibly lifelong influences on subsequent behavior. Social subjugation is thus likely to be a prime determinant of inter-individual behavioral differences in crickets. Our work also opens new avenues for investigating proximate mechanisms underlying depression-like phenomena.
format Online
Article
Text
id pubmed-5598953
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-55989532017-09-22 Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system Rose, Jacqueline Rillich, Jan Stevenson, Paul A. PLoS One Research Article Losing a fight against a conspecific male (social defeat) induces a period of suppressed aggressiveness and general behaviour, often with symptoms common to human psychiatric disorders. Agonistic experience is also discussed as a potential cause of consistent, behavioral differences between individuals (animal “personality”). In non-mammals, however, the impact of single agonistic encounters typically last only hours, but then again studies of repeated intermittent defeat (chronic social defeat) are seldom. We report the effect of chronic social defeat in adult male crickets (Gryllus bimaculatus), for which all known behavioral effects of defeat last only 3 h. Firstly, after 48 h social isolation, crickets that experienced 5 defeats at 24 h intervals against the same, weight-matched opponent exhibited suppressed aggressiveness lasting >24 h, which was still evident when the animals were matched against an unfamiliar opponent at the last trial. Secondly, this longer-term depression of aggression also occurred in 48 h isolated crickets that lost 6 fights at 1 h intervals against unfamiliar opponents at each trial. Thirdly, crickets isolated as larvae until adult maturity (>16 days) were significantly more aggressive, and less variable in their aggressiveness at their very first fight than 48 h isolates, and also significantly more resilient to the effects of chronic social defeat. We conclude that losing an aggressive encounter in crickets has a residual effect, lasting at least 24 h, that accumulates when repeated defeats are experienced, and leads to a prolonged depression of aggressive motivation in subordinates. Furthermore, our data indicate that social interactions between young adults and possibly larvae can have even longer, possibly lifelong influences on subsequent behavior. Social subjugation is thus likely to be a prime determinant of inter-individual behavioral differences in crickets. Our work also opens new avenues for investigating proximate mechanisms underlying depression-like phenomena. Public Library of Science 2017-09-14 /pmc/articles/PMC5598953/ /pubmed/28910319 http://dx.doi.org/10.1371/journal.pone.0184121 Text en © 2017 Rose et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rose, Jacqueline
Rillich, Jan
Stevenson, Paul A.
Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title_full Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title_fullStr Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title_full_unstemmed Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title_short Chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
title_sort chronic social defeat induces long-term behavioral depression of aggressive motivation in an invertebrate model system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5598953/
https://www.ncbi.nlm.nih.gov/pubmed/28910319
http://dx.doi.org/10.1371/journal.pone.0184121
work_keys_str_mv AT rosejacqueline chronicsocialdefeatinduceslongtermbehavioraldepressionofaggressivemotivationinaninvertebratemodelsystem
AT rillichjan chronicsocialdefeatinduceslongtermbehavioraldepressionofaggressivemotivationinaninvertebratemodelsystem
AT stevensonpaula chronicsocialdefeatinduceslongtermbehavioraldepressionofaggressivemotivationinaninvertebratemodelsystem