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1.
Proc Natl Acad Sci U S A ; 119(12): e2114230119, 2022 03 22.
Article in English | MEDLINE | ID: mdl-35286206

ABSTRACT

For group-living animals, the social environment provides salient experience that can weaken or strengthen aspects of cognition such as memory recall. Although the cellular substrates of individually acquired fear memories in the dentate gyrus (DG) and basolateral amygdala (BLA) have been well-studied and recent work has revealed circuit mechanisms underlying the encoding of social experience, the processes by which social experience interacts with an individual's memories to alter recall remain unknown. Here we show that stressful social experiences enhance the recall of previously acquired fear memories in male but not female mice, and that social buffering of conspecifics' distress blocks this enhancement. Activity-dependent tagging of cells in the DG during fear learning revealed that these ensembles were endogenously reactivated during the social experiences in males, even after extinction. These reactivated cells were shown to be functional components of engrams, as optogenetic stimulation of the cells active during the social experience in previously fear-conditioned and not naïve animals was sufficient to drive fear-related behaviors. Taken together, our findings suggest that social experiences can reactivate preexisting engrams to thereby strengthen discrete memories.


Subject(s)
Fear , Memory , Social Interaction , Animals , Fear/physiology , Hippocampus/physiology , Learning/physiology , Memory/physiology , Mental Recall/physiology
2.
Curr Biol ; 29(11): 1885-1894.e4, 2019 06 03.
Article in English | MEDLINE | ID: mdl-31130452

ABSTRACT

Emerging evidence indicates that distinct hippocampal domains differentially drive cognition and emotion [1, 2]; dorsal regions encode spatial, temporal, and contextual information [3-5], whereas ventral regions regulate stress responses [6], anxiety-related behaviors [7, 8], and emotional states [8-10]. Although previous studies demonstrate that optically manipulating cells in the dorsal hippocampus can drive the behavioral expression of positive and negative memories, it is unknown whether changes in cellular activity in the ventral hippocampus can drive such behaviors [11-14]. Investigating the extent to which distinct hippocampal memories across the longitudinal axis modulate behavior could aid in the understanding of stress-related psychiatric disorders known to affect emotion, memory, and cognition [15]. Here, we asked whether tagging and stimulating cells along the dorsoventral axis of the hippocampus could acutely, chronically, and differentially promote context-specific behaviors. Acute reactivation of both dorsal and ventral hippocampus cells that were previously active during memory formation drove freezing behavior, place avoidance, and place preference. Moreover, chronic stimulation of dorsal or ventral hippocampal fear memories produced a context-specific reduction or enhancement of fear responses, respectively, thus demonstrating bi-directional and context-specific modulation of memories along the longitudinal axis of the hippocampus. Fear memory suppression was associated with a reduction in hippocampal cells active during retrieval, while fear memory enhancement was associated with an increase in basolateral amygdala activity. Together, our data demonstrate that discrete sets of cells throughout the hippocampus provide key nodes sufficient to bi-directionally reprogram both the neural and behavioral expression of memory.


Subject(s)
Hippocampus/physiology , Memory/physiology , Neurons/physiology , Animals , Conditioning, Classical , Fear/physiology , Male , Mental Recall/physiology , Mice , Mice, Inbred C57BL , Random Allocation
3.
Sci Rep ; 9(1): 5393, 2019 04 01.
Article in English | MEDLINE | ID: mdl-30931967

ABSTRACT

Foraging exposes organisms to rewarding and aversive events, providing a selective advantage for maximizing the former while minimizing the latter. Honey bees (Apis mellifera) associate environmental stimuli with appetitive or aversive experiences, forming preferences for scents, locations, and visual cues. Preference formation is influenced by inter-individual variation in sensitivity to rewarding and aversive stimuli, which can be modulated by pharmacological manipulation of biogenic amines. We propose that foraging experiences act on biogenic amine pathways to induce enduring changes to stimulus responsiveness. To simulate varied foraging conditions, freely-moving bees were housed in cages where feeders offered combinations of sucrose solution, floral scents, and aversive electric shock. Transient effects were excluded by providing bees with neutral conditions for three days prior to all subsequent assays. Sucrose responsiveness was reduced in bees that had foraged for scented rather than unscented sucrose under benign conditions. This was not the case under aversive foraging conditions, suggesting an adaptive tuning process which maximizes preference for high quality, non-aversive floral sites. Foraging conditions also influenced antennal lobe octopamine and serotonin, neuromodulators involved in stimulus responsiveness and foraging site evaluation. Our results suggest that individuals' foraging experiences durably modify neurochemistry and shape future foraging behaviour.


Subject(s)
Bees/physiology , Biogenic Amines/metabolism , Feeding Behavior/physiology , Mushroom Bodies/metabolism , Neuropil/metabolism , Sucrose/administration & dosage , Animals , Appetitive Behavior/drug effects , Appetitive Behavior/physiology , Arthropod Antennae/drug effects , Arthropod Antennae/physiology , Octopamine/metabolism , Odorants , Reward
4.
Sci Rep ; 8(1): 17764, 2018 12 10.
Article in English | MEDLINE | ID: mdl-30531822

ABSTRACT

Eusocial insects divide their labour so that individuals working inside the nest are affected by external conditions through a cascade of social interactions. Honey bees (Apis mellifera) transfer food and information via mouth-to-mouth social feeding, ie trophallaxis, a process known to be modulated by the rate of food flow at feeders and familiarity of food's scent. Little is understood about how aversive foraging conditions such as predation and con-specific competition affect trophallaxis. We hypothesized that aversive conditions have an impact on food transfer inside the colony. Here we explore the effect of foragers' aversive experience on downstream trophallaxis in a cage paradigm. Each cage contained one group of bees that was separated from feeders by mesh and allowed to feed only through trophallaxis, and another group that had access to feeders and self-specialized to either forage or distribute food. Our results show that aversive foraging conditions increase non-foragers' trophallaxis with bees restricted from feeder access when food is scented, and have the opposite effect when food is unscented. We discuss potential behavioural mechanisms and implications for the impact of aversive conditions such as malaise inducing toxins, predation, and con-specific competition.


Subject(s)
Behavior, Animal/physiology , Feeding Behavior/physiology , Affect/physiology , Animals , Bees/physiology , Food , Odorants , Predatory Behavior/physiology , Social Behavior
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