The Ventral Hippocampus Controls Stress-Provoked Impulsive Aggression through the Ventromedial Hypothalamus in Post-Weaning Social Isolation Mice

Chang, Chih Hua; Gean, Po Wu

doi:10.1016/j.celrep.2019.07.005

Cited by 70 publications

(62 citation statements)

References 58 publications

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“…Foot shock is a commonly used procedure to induce traumatic stress in rodents (Rau et al, 2005;Bali and Jaggi, 2015;Chang et al, 2015Chang et al, , 2018Chang and Gean, 2019;Brivio et al, 2020). We adopted a foot shock protocol from Rau et al (2005).…”

Section: Foot Shock and Contextual Fear Memory Testmentioning

confidence: 99%

“…Previous studies show that attack behavior increases at 30 min after traumatic stress induced by electric foot shock (Chang et al, 2015(Chang et al, , 2018Chang and Gean, 2019). To test whether the aggression increase following traumatic stress is long lasting, we administered a traumatic stress protocol by delivering 15-foot shocks at 0.4 mA randomly spaced over a 90-min period (Rau et al, 2005).…”

Section: Traumatic Stress Induces Prolonged Increases In Aggressionmentioning

confidence: 99%

“…Aggression can be influenced by prior agonistic and stressful experience. For example, in rodents, stressful life experience such as social deprivation can instigate unprovoked attack behavior, and this effect is exacerbated by traumatic stress induced by foot shock (Veenema, 2009;Toth et al, 2011;Chang et al, 2015Chang et al, , 2018Zelikowsky et al, 2018;Chang and Gean, 2019). In humans, traumatic stress may trigger acute stress disorder and PTSD, and individuals with PTSD may exhibit increased aggression that lasts for years after the initial stressor (Nelson and Trainor, 2007;McHugh et al, 2012;American Psychiatric Association, 2013;Smerin et al, 2016;Taft et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…All three areas are activated by stress, and the VmH and BNST have been shown to regulate aggressive responses to perceived threats (Silva et al, 2013;Anthony et al, 2014;Butler et al, 2015;Miller et al, 2019). The VmH in particular mediates the acute increase in aggression after foot shock (Chang and Gean, 2019). Based on these findings, it is intriguing to test whether these MeA target areas are involved in traumatic stress-induced prolonged aggression increase.…”

Section: Introductionmentioning

confidence: 99%

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Traumatic Stress Induces Prolonged Aggression Increase through Synaptic Potentiation in the Medial Amygdala Circuits

Nordman

2020

eNeuro

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Traumatic stress can lead to heightened aggression which may be a symptom of psychiatric diseases such as PTSD and intermittent explosive disorder. The medial amygdala (MeA) is an evolutionarily conserved subnucleus of the amygdala that regulates attack behavior and behavioral responses to stressors. The precise contribution of the MeA in traumatic stress-induced aggression, however, requires further elucidation. In this study, we used foot shock to induce traumatic stress in mice and examine the mechanisms of prolonged aggression increase associated with it. Foot shock causes a prolonged increase in aggression that lasts at least one week. In vivo electrophysiological recordings revealed that foot shock induces potentiation of synapses formed between the MeA and the ventromedial hypothalamus (VmH) and bed nucleus of the stria terminalis (BNST). This synaptic potentiation lasts at least one week. Induction of synaptic depotentiation with low-frequency photostimulation (LFPS) immediately after foot shock suppresses the prolonged aggression increase without affecting non-aggressive social behavior, anxiety-like and depression-like behaviors, or fear learning. These results show that potentiation of the MeA-VmH and MeA-BNST circuits is essential for traumatic stress to cause a prolonged increase in aggression. These circuits may be potential targets for the development of therapeutic strategies to treat the aggression symptom associated with psychiatric diseases.

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Section: Foot Shock and Contextual Fear Memory Testmentioning

confidence: 99%

Section: Traumatic Stress Induces Prolonged Increases In Aggressionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Traumatic Stress Induces Prolonged Aggression Increase through Synaptic Potentiation in the Medial Amygdala Circuits

Nordman

2020

eNeuro

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“…Within the vHPC, functional specialization is delineated into distinct subsets of neurons that project to specific limbic structures to mediate unique aspects of behavior 9,13,[17][18][19][20][21][22][23][24] . One such functional distinction has recently been identified between the projections to the lateral hypothalamus (LHA) and basal amygdala (BA), wherein ventral hippocampal CA1 (vCA1) projections to the BA, but not LHA, are necessary for contextual fear conditioning 9 .…”

mentioning

confidence: 99%

Contextual fear memory retrieval by correlated ensembles of ventral CA1 neurons

et al. 2020

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Ventral hippocampal CA1 (vCA1) projections to the amygdala are necessary for contextual fear memory. Here we used in vivo Ca 2+ imaging in mice to assess the temporal dynamics by which ensembles of vCA1 neurons mediate encoding and retrieval of contextual fear memories. We found that a subset of vCA1 neurons were responsive to the aversive shock during context conditioning, their activity was necessary for memory encoding, and these shockresponsive neurons were enriched in the vCA1 projection to the amygdala. During memory retrieval, a population of vCA1 neurons became correlated with shock-encoding neurons, and the magnitude of synchronized activity within this population was proportional to memory strength. The emergence of these correlated networks was disrupted by inhibiting vCA1 shock responses during memory encoding. Thus, our findings suggest that networks of cells that become correlated with shock-responsive neurons in vCA1 are essential components of contextual fear memory ensembles.

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Adult Neurogenesis and the Initiation of Social Aggression in Male Mice

Tsuda,

Akoh‐Arrey,

Mercurio

et al. 2024

Hippocampus

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The hippocampus is important for social behavior and exhibits unusual structural plasticity in the form of continued production of new granule neurons throughout adulthood, but it is unclear how adult neurogenesis contributes to social interactions. In the present study, we suppressed neurogenesis using a pharmacogenetic mouse model and examined social investigation and aggression in adult male mice to investigate the role of hippocampal adult‐born neurons in the expression of aggressive behavior. In simultaneous choice tests with stimulus mice placed in corrals, mice with complete suppression of adult neurogenesis in adulthood (TK mice) exhibited normal social investigation behaviors, indicating that new neurons are not required for social interest, social memory, or detection of and response to social olfactory signals. However, mice with suppressed neurogenesis displayed decreased offensive and defensive aggression in a resident‐intruder paradigm, and less resistance in a social dominance test, relative to neurogenesis‐intact controls, when paired with weight and strain‐matched (CD‐1) mice. During aggression tests, TK mice were frequently attacked by the CD‐1 intruder mice, which never occurred with WTs, and normal CD‐1 male mice investigated TK mice less than controls when corralled in the social investigation test. Importantly, TK mice showed normal aggression toward prey (crickets) and smaller, nonaggressive (olfactory bulbectomized) C57BL/6J intruders, suggesting that mice lacking adult neurogenesis do not avoid aggressive social interactions if they are much larger than their opponent and will clearly win. Taken together, our findings show that adult hippocampal neurogenesis plays an important role in the instigation of intermale aggression, possibly by weighting a cost–benefit analysis against confrontation in cases where the outcome of the fight is not clear.

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The Ventral Hippocampus Controls Stress-Provoked Impulsive Aggression through the Ventromedial Hypothalamus in Post-Weaning Social Isolation Mice

Cited by 70 publications

References 58 publications

Traumatic Stress Induces Prolonged Aggression Increase through Synaptic Potentiation in the Medial Amygdala Circuits

Traumatic Stress Induces Prolonged Aggression Increase through Synaptic Potentiation in the Medial Amygdala Circuits

Contextual fear memory retrieval by correlated ensembles of ventral CA1 neurons

Adult Neurogenesis and the Initiation of Social Aggression in Male Mice

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