scholarly journals Dynamic encoding of social threat and spatial context in the hypothalamus

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Piotr Krzywkowski ◽  
Beatrice Penna ◽  
Cornelius T Gross
Keyword(s):  
Internal State ◽  
Social Defeat ◽  
Ventromedial Hypothalamus ◽  
Social Aggression ◽  
Spatial Context ◽  
Social Threat ◽  
Firing Activity ◽  
Functional Reorganization ◽  
General Internal ◽  
Defensive Behaviors

Social aggression and avoidance are defensive behaviors expressed by territorial animals in a manner appropriate to spatial context and experience. The ventromedial hypothalamus controls both social aggression and avoidance, suggesting that it may encode a general internal state of threat modulated by space and experience. Here, we show that neurons in the mouse ventromedial hypothalamus are activated both by the presence of a social threat as well as by a chamber where social defeat previously occurred. Moreover, under conditions where the animal could move freely between a home and defeat chamber, firing activity emerged that predicted the animal’s position, demonstrating the dynamic encoding of spatial context in the hypothalamus. Finally, we found that social defeat induced a functional reorganization of neural activity as optogenetic activation could elicit avoidance after, but not before social defeat. These findings reveal how the hypothalamus dynamically encodes spatial and sensory cues to drive social behaviors.

scholarly journals Dynamic encoding of social threat and spatial context in the hypothalamus

2019 ◽  
Author(s):  
Piotr Krzywkowski ◽  
Beatrice Penna ◽  
Cornelius T. Gross
Keyword(s):  
Internal State ◽  
Social Defeat ◽  
Ventromedial Hypothalamus ◽  
Spatial Context ◽  
Social Threat ◽  
Sensory Cues ◽  
Dominance Status ◽  
Functional Reorganization ◽  
Instinctive Behavior

AbstractTerritorial animals must be able to express social aggression or avoidance in a manner appropriate to spatial context and dominance status. Recent studies indicate that the ventromedial hypothalamus controls both innate aggression and avoidance, suggesting that it may encode an internal state of threat common to both behaviors. Here we used single unit in vivo calcium microendoscopy to identify neurons in the mouse ventromedial hypothalamus encoding social threat. Threat neurons were activated during social defeat as well as when the animal performed risk assessment. Unexpectedly, threat neurons were also activate in the chamber where the animal had been previously defeated and a distinct set of neurons emerged that were active in its home chamber, demonstrating the dynamic encoding of spatial context in the hypothalamus. Ensemble analysis of neural activity showed that social defeat induced a change in the encoding of social information and optogenetic activation of ventromedial hypothalamus neurons was able to elicit avoidance after, but not before social defeat, demonstrating a functional reorganization of the pathway by social experience. These findings reveal how instinctive behavior circuits in the hypothalamus dynamically encode spatial and sensory cues to drive adaptive social behaviors.

scholarly journals Stimulus-specific neural encoding of a persistent, internal defensive state in the hypothalamus

2019 ◽  
Author(s):  
Ann Kennedy ◽  
Prabhat S. Kunwar ◽  
Lingyun Li ◽  
Daniel Wagenaar ◽  
David J. Anderson
Keyword(s):  
Neural Activity ◽  
Internal State ◽  
Stress Hormones ◽  
Ventromedial Hypothalamus ◽  
Persistent Activity ◽  
Neural Encoding ◽  
Population Activity ◽  
Defensive Responses ◽  
Neuroendocrine Mechanisms ◽  
Threatening Stimuli

SummaryPersistent neural activity has been described in cortical, hippocampal, and motor networks as mediating short-term working memory of transiently encountered stimuli1–4. Internal emotion states such as fear also exhibit persistence following exposure to an inciting stimulus5,6, but such persistence is typically attributed to circulating stress hormones7–9; whether persistent neural activity also plays a role has not been established. SF1+/Nr5a1+ neurons in the dorsomedial and central subdivision of the ventromedial hypothalamus (VMHdm/c) are necessary for innate and learned defensive responses to predators10–13. Optogenetic activation of VMHdmSF1 neurons elicits defensive behaviors that can outlast stimulation11,14, suggesting it induces a persistent internal state of fear or anxiety. Here we show that VMHdmSF1 neurons exhibit persistent activity lasting tens of seconds, in response to naturalistic threatening stimuli. This persistent activity was correlated with, and required for, persistent thigmotaxic (anxiety-like) behavior in an open-field assay. Microendoscopic imaging of VMHdmSF1 neurons revealed that persistence reflects dynamic temporal changes in population activity, rather than simply synchronous, slow decay of simultaneously activated neurons. Unexpectedly, distinct but overlapping VMHdmSF1 subpopulations were persistently activated by different classes of threatening stimuli. Computational modeling suggested that recurrent neural networks (RNNs) incorporating slow excitation and a modest degree of neurochemical or spatial bias can account for persistent activity that maintains stimulus identity, without invoking genetically determined “labeled lines”15. Our results provide causal evidence that persistent neural activity, in addition to well-established neuroendocrine mechanisms, can contribute to the ability of emotion states to outlast their inciting stimuli, and suggest a mechanism that could prevent over-generalization of defensive responses without the need to evolve hardwired circuits specific for each type of threat.

Site familiarity affects antipredator behavior of the amphisbaenian Blanus cinereus

2000 ◽  
Vol 78 (12) ◽  
pp. 2142-2146 ◽  
Author(s):  
Pilar López ◽  
José Martín ◽  
Andrés Barbosa
Keyword(s):  
Body Temperature ◽  
Home Range ◽  
Internal State ◽  
Antipredator Behavior ◽  
Soil Surface ◽  
Site Familiarity ◽  
Morphological Adaptations ◽  
Defensive Behaviors ◽  
Antipredator Behaviors ◽  
Tongue Flicks

Morphological adaptations of amphisbaenians to fossorial life might affect their antipredator-behavior decisions. Amphisbaenians exposed on the soil surface by a predator can escape by burrowing immediately or by using alternative defensive behaviors on the soil surface, and should decide where to burrow in order to return to their home range. We simulated in the laboratory predatory attacks toward individual amphisbaenians (Blanus cinereus), and examined whether their antipredator and burrowing responses were affected by site familiarity (familiar versus unfamiliar substrate) and their internal state (i.e., body temperature and associated burrowing performance). Amphisbaenians showed significantly longer episodes of alternative antipredator behaviors on the soil surface (coiling and still) when the temperature was low. Before starting to burrow in unfamiliar substrates, individuals emitted numerous tongue flicks and moved for significantly longer periods of time than when on familiar substrates, independently of temperature. In contrast, in their own cages, with familiar substrates, amphisbaenians performed only a few tongue flicks before starting to burrow. Subsequently, the time spent burrowing was significantly longer when the temperature was low or amphisbaenians were on an unfamiliar substrate. These results suggest that amphisbaenians are able to recognize their own home range by chemosensory cues and that they are able to use this information when deciding where to burrow to escape from potential predators.

scholarly journals Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus

2021 ◽  
Author(s):  
Ryan Rahy ◽  
Hiroki Asari ◽  
Cornelius T. Gross
Keyword(s):  
Sensory Input ◽  
Functional Organization ◽  
Cell Activity ◽  
Ventromedial Hypothalamus ◽  
Feedback Circuit ◽  
Neural Firing ◽  
Firing Activity ◽  
Local Circuit ◽  
Inhibitory Feedback

AbstractThe mouse ventromedial hypothalamus (VMH) is both necessary and sufficient for defensive responses to predator and social threats. Defensive behaviors typically involve cautious approach toward potentially threatening stimuli aimed at obtaining information about the risk involved, followed by sudden avoidance and flight behavior to escape harm. In vivo neural recording studies in mice have identified two major populations of VMH neurons that either increase their firing activity as the animal approaches the threat (called Assessment+ cells) or increase their activity as the animal flees the threat (called Flight+ cells). Interestingly, Assessment+ and Flight+ cells abruptly decrease and increase their firing activity, respectively, at the decision point for flight, creating an escape-related “switch” in functional state. This suggests that the activity of the two cell types in VMH is coordinated and could result from local circuit interactions. Here, we used computational modelling to test if a local inhibitory feedback circuit could give rise to key features of the neural activity seen in VMH during the approach-to-flight transition. Starting from a simple dual-population inhibitory feedback circuit receiving repeated trains of monotonically increasing sensory input to mimic approach to threat, we tested the requirement for balanced sensory input, balanced feedback, short-term synaptic plasticity, rebound excitation, and inhibitory feedback exclusivity to reproduce an abrupt, sensory-thresholded reciprocal firing change that resembles Assessment+ and Flight+ cell activity seen in vivo. Our work demonstrates that a relatively simple local circuit architecture is sufficient for the emergence of firing patterns similar to those seen in vivo and suggests that a reiterative process of experimental and computational work may be a fruitful avenue for better understanding the functional organization of mammalian instinctive behaviors at the circuit level.

scholarly journals Collateral Pathways from the Ventromedial Hypothalamus Mediate Defensive Behaviors

Neuron ◽  
2015 ◽  
Vol 85 (6) ◽  
pp. 1344-1358 ◽  
Author(s):  
Li Wang ◽  
Irene Z. Chen ◽  
Dayu Lin
Keyword(s):  
Ventromedial Hypothalamus ◽  
Defensive Behaviors ◽  
Collateral Pathways

scholarly journals Reconceptualising resilience within a translational framework is supported by unique and brain-region specific transcriptional signatures in mice

2020 ◽  
Author(s):  
Sarah Ayash ◽  
Thomas Lingner ◽  
Soojin Ryu ◽  
Raffael Kalisch ◽  
Ulrich Schmitt ◽  
...  
Keyword(s):  
Fear Conditioning ◽  
Brain Region ◽  
Social Defeat ◽  
Brain Regions ◽  
Social Threat ◽  
Social Avoidance ◽  
Human Data ◽  
Conditioned Learning ◽  
Aversive Response ◽  
Dichotomous Classification

ABSTRACTChronic social defeat (CSD) in mice has been increasingly employed in experimental resilience research. Particularly, the degree of CSD-induced social avoidance is used to classify animals into resilient (socially non-avoidant) versus susceptible (avoidant). In-spired by human data pointing to threat-safety discrimination and responsiveness to extinction training of aversive memories as characteristics of resilient individuals, we here describe a translationally informed stratification which identified three phenotypic subgroups of mice following CSD: the Discriminating-avoiders, characterised by successful social threat-safety discrimination and successful extinction of social avoidance; the Indis-criminate-avoiders, showing aversive response generalisation, and the Non-avoiders (absence of social avoidance) displaying impaired conditioned learning. Furthermore, and supporting the biological validity of our approach, we uncovered subgroup-specific transcriptional signatures in classical fear conditioning and anxiety-related brain regions. Our reconceptualisation of resilience in mice refines the currently used dichotomous classification and contributes to advancing future translational approaches.

scholarly journals Differential encoding of predator fear in the ventromedial hypothalamus and periaqueductal grey

2018 ◽  
Author(s):  
Maria Esteban Masferrer ◽  
Bianca A. Silva ◽  
Kensaku Nomoto ◽  
Susana Q. Lima ◽  
Cornelius T. Gross
Keyword(s):  
Internal State ◽  
Motor Pattern ◽  
Ventromedial Hypothalamus ◽  
Sympathetic Activation ◽  
Periaqueductal Grey ◽  
Differential Encoding ◽  
Defensive Responses ◽  
Electrophysiological Recordings ◽  
Mammalian Predator ◽  
Stimulation Of

AbstractThe ventromedial hypothalamus is a central node of the mammalian predator defense network. Stimulation of this structure in rodents and primates elicits abrupt defensive responses, including flight, freezing, sympathetic activation, and panic, while inhibition reduces defensive responses to predators. The major efferent target of the ventromedial hypothalamus is the dorsal periaqueductal grey, and stimulation of this structure also elicits flight, freezing, and sympathetic activation. However, reversible inhibition experiments suggest that the ventromedial hypothalamus and periaqueductal grey play distinct roles in the control of defensive behavior, with the former proposed to encode an internal state necessary for the motivation of defensive responses, while the latter serves as a motor pattern initiator. Here we used electrophysiological recordings of single units in behaving mice exposed to a rat to investigate the encoding of predator fear in the dorsomedial division of the ventromedial hypothalamus and the dorsal periaqueductal grey. Distinct correlates of threat intensity and motor responses were found in both structures, suggesting a distributed encoding of sensory and motor features in the medial hypothalamic-brainstem instinctive network.

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