Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus

Activation of Esr1 + neurons of the mouse ventromedial hypothalamus initiates graded social behavioural responses–weak activation triggers close investigation (sniffing) during a social encounter that often leads, with continued stimulation, to mounting behaviours by males towards either gender; mou...

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Published inNature (London) Vol. 509; no. 7502; pp. 627 - 632
Main Authors Lee, Hyosang, Kim, Dong-Wook, Remedios, Ryan, Anthony, Todd E., Chang, Angela, Madisen, Linda, Zeng, Hongkui, Anderson, David J.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 29.05.2014
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Abstract Activation of Esr1 + neurons of the mouse ventromedial hypothalamus initiates graded social behavioural responses–weak activation triggers close investigation (sniffing) during a social encounter that often leads, with continued stimulation, to mounting behaviours by males towards either gender; mounting behaviour transitions to aggressive attacks with greater stimulation intensity. Hypothalamus neurons that mediate aggression In the mouse ventromedial hypothalamus, there are intermixed populations of neurons differentiated by the expression of the oestrogen receptor, Esr1. Previous work revealed that Esr1 + neurons can initiate aggressive behaviour when artificially activated. Here, David Anderson and colleagues extend those results to demonstrate a graded behavioural response to the activation of these neurons along a continuum of social behavior. Weaker activation could initiate close inspection during an encounter that could lead to mounting behaviours by males towards either gender with further stimulation. Mounting behaviour transitioned to aggressive attacks with even greater stimulation intensity. Thus, these data reveal a circuit that controls the nature of a set of social behaviors in a scalable manner based on neuronal activity levels. Social behaviours, such as aggression or mating, proceed through a series of appetitive and consummatory phases 1 that are associated with increasing levels of arousal 2 . How such escalation is encoded in the brain, and linked to behavioural action selection, remains an unsolved problem in neuroscience. The ventrolateral subdivision of the murine ventromedial hypothalamus (VMHvl) contains neurons whose activity increases during male–male and male–female social encounters. Non-cell-type-specific optogenetic activation of this region elicited attack behaviour, but not mounting 3 . We have identified a subset of VMHvl neurons marked by the oestrogen receptor 1 (Esr1), and investigated their role in male social behaviour. Optogenetic manipulations indicated that Esr1 + (but not Esr1 − ) neurons are sufficient to initiate attack, and that their activity is continuously required during ongoing agonistic behaviour. Surprisingly, weaker optogenetic activation of these neurons promoted mounting behaviour, rather than attack, towards both males and females, as well as sniffing and close investigation. Increasing photostimulation intensity could promote a transition from close investigation and mounting to attack, within a single social encounter. Importantly, time-resolved optogenetic inhibition experiments revealed requirements for Esr1 + neurons in both the appetitive (investigative) and the consummatory phases of social interactions. Combined optogenetic activation and calcium imaging experiments in vitro , as well as c-Fos analysis in vivo , indicated that increasing photostimulation intensity increases both the number of active neurons and the average level of activity per neuron. These data suggest that Esr1 + neurons in VMHvl control the progression of a social encounter from its appetitive through its consummatory phases, in a scalable manner that reflects the number or type of active neurons in the population.
AbstractList Activation of Esr1 + neurons of the mouse ventromedial hypothalamus initiates graded social behavioural responses–weak activation triggers close investigation (sniffing) during a social encounter that often leads, with continued stimulation, to mounting behaviours by males towards either gender; mounting behaviour transitions to aggressive attacks with greater stimulation intensity. Hypothalamus neurons that mediate aggression In the mouse ventromedial hypothalamus, there are intermixed populations of neurons differentiated by the expression of the oestrogen receptor, Esr1. Previous work revealed that Esr1 + neurons can initiate aggressive behaviour when artificially activated. Here, David Anderson and colleagues extend those results to demonstrate a graded behavioural response to the activation of these neurons along a continuum of social behavior. Weaker activation could initiate close inspection during an encounter that could lead to mounting behaviours by males towards either gender with further stimulation. Mounting behaviour transitioned to aggressive attacks with even greater stimulation intensity. Thus, these data reveal a circuit that controls the nature of a set of social behaviors in a scalable manner based on neuronal activity levels. Social behaviours, such as aggression or mating, proceed through a series of appetitive and consummatory phases 1 that are associated with increasing levels of arousal 2 . How such escalation is encoded in the brain, and linked to behavioural action selection, remains an unsolved problem in neuroscience. The ventrolateral subdivision of the murine ventromedial hypothalamus (VMHvl) contains neurons whose activity increases during male–male and male–female social encounters. Non-cell-type-specific optogenetic activation of this region elicited attack behaviour, but not mounting 3 . We have identified a subset of VMHvl neurons marked by the oestrogen receptor 1 (Esr1), and investigated their role in male social behaviour. Optogenetic manipulations indicated that Esr1 + (but not Esr1 − ) neurons are sufficient to initiate attack, and that their activity is continuously required during ongoing agonistic behaviour. Surprisingly, weaker optogenetic activation of these neurons promoted mounting behaviour, rather than attack, towards both males and females, as well as sniffing and close investigation. Increasing photostimulation intensity could promote a transition from close investigation and mounting to attack, within a single social encounter. Importantly, time-resolved optogenetic inhibition experiments revealed requirements for Esr1 + neurons in both the appetitive (investigative) and the consummatory phases of social interactions. Combined optogenetic activation and calcium imaging experiments in vitro , as well as c-Fos analysis in vivo , indicated that increasing photostimulation intensity increases both the number of active neurons and the average level of activity per neuron. These data suggest that Esr1 + neurons in VMHvl control the progression of a social encounter from its appetitive through its consummatory phases, in a scalable manner that reflects the number or type of active neurons in the population.
Social behaviors, such as aggression or mating, proceed through a series of appetitive and consummatory phases 1 that are associated with increasing levels of arousal 2 . How such escalation is encoded in the brain, and linked to behavioral action selection, remains an important unsolved problem in neuroscience. The ventrolateral subdivision of the murine ventromedial hypothalamus (VMHvl) contains neurons whose activity increases during male-male and male-female social encounters. Non-cell type-specific optogenetic activation of this region elicited attack behavior, but not mounting 3 . We have identified a subset of VMHvl neurons marked by the estrogen receptor 1 (Esr1), and investigated their role in male social behavior. Optogenetic manipulations indicated that Esr1 + (but not Esr1 - ) neurons are sufficient to initiate attack, and that their activity is continuously required during ongoing agonistic behavior. Surprisingly, weaker optogenetic activation of these neurons promoted mounting behavior, rather than attack, towards both males and females, as well as sniffing and close investigation (CI). Increasing photostimulation intensity could promote a transition from CI and mounting to attack, within a single social encounter. Importantly, time-resolved optogenetic inhibition experiments revealed requirements for Esr1 + neurons in both the appetitive (investigative) and the consummatory phases of social interactions. Combined optogenetic activation and calcium imaging experiments in vitro , as well as c-Fos analysis in vivo , indicated that increasing photostimulation intensity increases both the number of active neurons and the average level of activity per neuron. These data suggest that Esr1 + neurons in VMHvl control the progression of a social encounter from its appetitive through its consummatory phases, in a scalable manner that reflects the number or type of active neurons in the population.
Social behaviours, such as aggression or mating, proceed through a series of appetitive and consummatory phases that are associated with increasing levels of arousal. How such escalation is encoded in the brain, and linked to behavioural action selection, remains an unsolved problem in neuroscience. The ventrolateral subdivision of the murine ventromedial hypothalamus (VMHvl) contains neurons whose activity increases during male-male and male-female social encounters. Non-cell-type-specific optogenetic activation of this region elicited attack behaviour, but not mounting. We have identified a subset of VMHvl neurons marked by the oestrogen receptor 1 (Esr1), and investigated their role in male social behaviour. Optogenetic manipulations indicated that Esr1(+) (but not Esr1(-)) neurons are sufficient to initiate attack, and that their activity is continuously required during ongoing agonistic behaviour. Surprisingly, weaker optogenetic activation of these neurons promoted mounting behaviour, rather than attack, towards both males and females, as well as sniffing and close investigation. Increasing photostimulation intensity could promote a transition from close investigation and mounting to attack, within a single social encounter. Importantly, time-resolved optogenetic inhibition experiments revealed requirements for Esr1(+) neurons in both the appetitive (investigative) and the consummatory phases of social interactions. Combined optogenetic activation and calcium imaging experiments in vitro, as well as c-Fos analysis in vivo, indicated that increasing photostimulation intensity increases both the number of active neurons and the average level of activity per neuron. These data suggest that Esr1(+) neurons in VMHvl control the progression of a social encounter from its appetitive through its consummatory phases, in a scalable manner that reflects the number or type of active neurons in the population.
Author Chang, Angela
Kim, Dong-Wook
Lee, Hyosang
Remedios, Ryan
Anthony, Todd E.
Anderson, David J.
Madisen, Linda
Zeng, Hongkui
AuthorAffiliation 4 Allen Institute for Brain Science, Seattle, WA 98103, USA
2 Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA
1 Division of Biology and Biological Engineering 156-29, California Institute of Technology, Pasadena, CA 91125, USA
3 Howard Hughes Medical Institute, Seattle, WA 98103, USA
AuthorAffiliation_xml – name: 4 Allen Institute for Brain Science, Seattle, WA 98103, USA
– name: 2 Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA
– name: 1 Division of Biology and Biological Engineering 156-29, California Institute of Technology, Pasadena, CA 91125, USA
– name: 3 Howard Hughes Medical Institute, Seattle, WA 98103, USA
Author_xml – sequence: 1
  givenname: Hyosang
  surname: Lee
  fullname: Lee, Hyosang
  organization: Division of Biology and Biological Engineering 156-29, California Institute of Technology, Howard Hughes Medical Institute
– sequence: 2
  givenname: Dong-Wook
  surname: Kim
  fullname: Kim, Dong-Wook
  organization: Computation and Neural Systems, California Institute of Technology
– sequence: 3
  givenname: Ryan
  surname: Remedios
  fullname: Remedios, Ryan
  organization: Division of Biology and Biological Engineering 156-29, California Institute of Technology
– sequence: 4
  givenname: Todd E.
  surname: Anthony
  fullname: Anthony, Todd E.
  organization: Division of Biology and Biological Engineering 156-29, California Institute of Technology
– sequence: 5
  givenname: Angela
  surname: Chang
  fullname: Chang, Angela
  organization: Division of Biology and Biological Engineering 156-29, California Institute of Technology
– sequence: 6
  givenname: Linda
  surname: Madisen
  fullname: Madisen, Linda
  organization: Allen Institute for Brain Science
– sequence: 7
  givenname: Hongkui
  surname: Zeng
  fullname: Zeng, Hongkui
  organization: Allen Institute for Brain Science
– sequence: 8
  givenname: David J.
  surname: Anderson
  fullname: Anderson, David J.
  email: wuwei@caltech.edu
  organization: Division of Biology and Biological Engineering 156-29, California Institute of Technology, Howard Hughes Medical Institute, Computation and Neural Systems, California Institute of Technology
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24739975$$D View this record in MEDLINE/PubMed
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Snippet Activation of Esr1 + neurons of the mouse ventromedial hypothalamus initiates graded social behavioural responses–weak activation triggers close investigation...
Social behaviours, such as aggression or mating, proceed through a series of appetitive and consummatory phases that are associated with increasing levels of...
Social behaviors, such as aggression or mating, proceed through a series of appetitive and consummatory phases 1 that are associated with increasing levels of...
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StartPage 627
SubjectTerms 13/1
14/19
42/41
631/378
64/60
9/74
Aggression - physiology
Animals
Estrogen Receptor alpha - metabolism
Female
Humanities and Social Sciences
Integrases - genetics
Integrases - metabolism
letter
Male
Mice
multidisciplinary
Neurons - metabolism
Optogenetics
Science
Sexual Behavior, Animal - physiology
Ventromedial Hypothalamic Nucleus - cytology
Ventromedial Hypothalamic Nucleus - physiology
Title Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus
URI https://link.springer.com/article/10.1038/nature13169
https://www.ncbi.nlm.nih.gov/pubmed/24739975
https://search.proquest.com/docview/1530951441
https://pubmed.ncbi.nlm.nih.gov/PMC4098836
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