scholarly journals Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Salvatore Lecca ◽  
Frank Julius Meye ◽  
Massimo Trusel ◽  
Anna Tchenio ◽  
Julia Harris ◽  
...  

A sudden aversive event produces escape behaviors, an innate response essential for survival in virtually all-animal species. Nuclei including the lateral habenula (LHb), the lateral hypothalamus (LH), and the midbrain are not only reciprocally connected, but also respond to negative events contributing to goal-directed behaviors. However, whether aversion encoding requires these neural circuits to ultimately prompt escape behaviors remains unclear. We observe that aversive stimuli, including foot-shocks, excite LHb neurons and promote escape behaviors in mice. The foot-shock-driven excitation within the LHb requires glutamatergic signaling from the LH, but not from the midbrain. This hypothalamic excitatory projection predominates over LHb neurons monosynaptically innervating aversion-encoding midbrain GABA cells. Finally, the selective chemogenetic silencing of the LH-to-LHb pathway impairs aversion-driven escape behaviors. These findings unveil a habenular neurocircuitry devoted to encode external threats and the consequent escape; a process that, if disrupted, may compromise the animal’s survival.

2022 ◽  
Vol 12 (1) ◽  
Author(s):  
Sarah Mondoloni ◽  
Manuel Mameli ◽  
Mauro Congiu

AbstractThroughout life, individuals experience a vast array of positive and aversive events that trigger adaptive behavioural responses. These events are often unpredicted and engage actions that are likely anchored on innate behavioural programs expressed by each individual member of virtually all animal species. In a second step, environmental cues, that are initially neutral, acquire value through the association with external sensory stimuli, and become instrumental to predict upcoming positive or negative events. This process ultimately prompts learned goal-directed actions allowing the pursuit of rewarding experience or the avoidance of a danger. Both innate and learned behavioural programs are evolutionarily conserved and fundamental for survival. Among the brain structures participating in the encoding of positive/negative stimuli and contributing to innate and learned behaviours is the epithalamic lateral habenula (LHb). The LHb provides top-down control of monoaminergic systems, responds to unexpected appetitive/aversive stimuli as well as external cues that predict the upcoming rewards or punishments. Accordingly, the LHb controls a number of behaviours that are innate (originating from unpredicted stimuli), and learned (stemming from predictive cues). In this review, we will discuss the progresses that rodent’s experimental work made in identifying how LHb activity governs these vital processes, and we will provide a view on how these findings integrate within a complex circuit connectivity.


2020 ◽  
Author(s):  
Bibi Nusreen Imambocus ◽  
Annika Wittich ◽  
Federico Tenedini ◽  
Fangmin Zhou ◽  
Chun Hu ◽  
...  

AbstractAnimals display a plethora of escape behaviors when faced with environmental threats. Selection of the appropriate response by the underlying neuronal network is key to maximize chances of survival. We uncovered a somatosensory network in Drosophila larvae that encodes two escape behaviors through input-specific neuropeptide action. Sensory neurons required for avoidance of noxious light and escape in response to harsh touch, each converge on discrete domains of the same neuromodulatory hub neurons. These gate harsh touch responses via short Neuropeptide F, but noxious light avoidance via compartmentalized, acute Insulin-like peptide 7 action and cognate Relaxin-family receptor signaling in connected downstream neurons. Peptidergic hub neurons can thus act as central circuit elements for first order processing of converging sensory inputs to gate specific escape responses.One Sentence SummaryCompartment-specific neuropeptide action regulates sensory information processing to elicit discrete escape behavior in Drosophila larvae.


2020 ◽  
Vol 43 (1) ◽  
pp. 417-439 ◽  
Author(s):  
Tiago Branco ◽  
Peter Redgrave

Escape is one of the most studied animal behaviors, and there is a rich normative theory that links threat properties to evasive actions and their timing. The behavioral principles of escape are evolutionarily conserved and rely on elementary computational steps such as classifying sensory stimuli and executing appropriate movements. These are common building blocks of general adaptive behaviors. Here we consider the computational challenges required for escape behaviors to be implemented, discuss possible algorithmic solutions, and review some of the underlying neural circuits and mechanisms. We outline shared neural principles that can be implemented by evolutionarily ancient neural systems to generate escape behavior, to which cortical encephalization has been added to allow for increased sophistication and flexibility in responding to threat.


2015 ◽  
Vol 27 (9) ◽  
pp. 1840-1853 ◽  
Author(s):  
Janine Bijsterbosch ◽  
Stephen Smith ◽  
Sonia J. Bishop

Sustained anxiety about potential future negative events is an important feature of anxiety disorders. In this study, we used a novel anticipation of shock paradigm to investigate individual differences in functional connectivity during prolonged threat of shock. We examined the correlates of between-participant differences in trait anxious affect and induced anxiety, where the latter reflects changes in self-reported anxiety resulting from the shock manipulation. Dissociable effects of trait anxious affect and induced anxiety were observed. Participants with high scores on a latent dimension of anxious affect showed less increase in ventromedial pFC–amygdala connectivity between periods of safety and shock anticipation. Meanwhile, lower levels of induced anxiety were linked to greater augmentation of dorsolateral pFC–anterior insula connectivity during shock anticipation. These findings suggest that ventromedial pFC–amygdala and dorsolateral pFC–insula networks might both contribute to regulation of sustained fear responses, with their recruitment varying independently across participants. The former might reflect an evolutionarily old mechanism for reducing fear or anxiety, whereas the latter might reflect a complementary mechanism by which cognitive control can be implemented to diminish fear responses generated due to anticipation of aversive stimuli or events. These two circuits might provide complementary, alternate targets for exploration in future pharmacological and cognitive intervention studies.


2016 ◽  
Vol 116 (3) ◽  
pp. 1161-1174 ◽  
Author(s):  
P. Leon Brown ◽  
Paul D. Shepard

The lateral habenula, a phylogenetically conserved epithalamic structure, is activated by aversive stimuli and reward omission. Excitatory efferents from the lateral habenula predominately inhibit midbrain dopamine neuronal firing through a disynaptic, feedforward inhibitory mechanism involving the rostromedial tegmental nucleus. However, the lateral habenula also directly targets dopamine neurons within the ventral tegmental area, suggesting that opposing actions may result from increased lateral habenula activity. In the present study, we tested the effect of habenular efferent stimulation on dopamine and nondopamine neurons in the ventral tegmental area of Sprague-Dawley rats using a parasagittal brain slice preparation. Single pulse stimulation of the fasciculus retroflexus excited 48% of dopamine neurons and 51% of nondopamine neurons in the ventral tegmental area of rat pups. These proportions were not altered by excision of the rostromedial tegmental nucleus and were evident in both cortical- and striatal-projecting dopamine neurons. Glutamate receptor antagonists blocked this excitation, and fasciculus retroflexus stimulation elicited evoked excitatory postsynaptic potentials with a nearly constant onset latency, indicative of a monosynaptic, glutamatergic connection. Comparison of responses in rat pups and young adults showed no significant difference in the proportion of neurons excited by fasciculus retroflexus stimulation. Our data indicate that the well-known, indirect inhibitory effect of lateral habenula activation on midbrain dopamine neurons is complemented by a significant, direct excitatory effect. This pathway may contribute to the role of midbrain dopamine neurons in processing aversive stimuli and salience.


2001 ◽  
Vol 280 (5) ◽  
pp. R1341-R1347 ◽  
Author(s):  
Takayoshi Hosono ◽  
Xiao-Ming Chen ◽  
Aya Miyatsuji ◽  
Tamae Yoda ◽  
Kyoko Yoshida ◽  
...  

Effects of estrogen on thermoregulatory vasomotion and heat-escape behavior were investigated in ovariectomized female rats supplemented with estrogen (replaced estrogen rats) or control saline (low estrogen rats). First, we measured tail temperature of freely moving rats at ambient temperatures (Ta) between 13 and 31°C. Tail temperature of the low estrogen rats was higher than that of the replaced estrogen rats at Ta between 19 and 25°C, indicating that the low estrogen rats exhibit more skin vasodilation than the replaced estrogen rats. There was no significant difference in oxygen consumption and core temperature between the two groups. Second, we analyzed heat-escape behaviors in a hot chamber where rats could obtain cold air by moving in and out of a reward area. The low estrogen rats kept Ta at a lower level than did the replaced estrogen rats. These results imply that the lack of estrogen facilitates heat dissipation both by skin vasodilation and by heat-escape behavior. Ovariectomized rats may mimic climacteric hot flushes not only for autonomic skin vasomotor activity but also for thermoregulatory behavior.


2000 ◽  
Vol 278 (1) ◽  
pp. R134-R139 ◽  
Author(s):  
Tamae Yoda ◽  
Larry I. Crawshaw ◽  
Kyoko Yoshida ◽  
Liu Su ◽  
Takayoshi Hosono ◽  
...  

Homeothermic animals regulate body temperature (Tb) by using both autonomic and behavioral mechanisms. In the latter process, animals seek out cooler or warmer places when they are exposed to excessively hot or cold environments. Thermoregulation is affected by the state of energy reserves in the body. In the present study, we examine the effects of 4-day food deprivation on circadian changes in Tb and on cold-escape and heat-escape behaviors in rats. Continuous measurement of Tb during food deprivation indicated that the peak Tb amplitude was not different from baseline values, but the trough amplitude continuously decreased after the onset of food deprivation. Cold-escape behavior was facilitated by food deprivation, whereas heat-escape behavior was unchanged. After the termination of food deprivation, the lowered Tb returned to normal on the first day. However, cold-escape behavior was still facilitated on the third day after food reintroduction. Autonomic and behavioral thermoregulatory effectors are modulated in the face of food shortage so as to maintain optimal performance during the active period, whereas increasing energy conservation occurs during the quiescent phase.


2021 ◽  
Author(s):  
Kinsey M Brock ◽  
Indiana E. Madden

Variation in color morph behavior is an important factor in the maintenance of color polymorphism. Alternative anti-predator behaviors are often associated with morphological traits such as coloration, possibly because predator-mediated viability selection favors certain combinations of anti-predator behavior and color. The Aegean wall lizard, Podarcis erhardii, is color polymorphic and populations can have up to three monochromatic morphs: orange, yellow, and white. We investigated whether escape behaviors differ among coexisting color morphs, and if morph behaviors are repeatable across different populations with the same predator species. Specifically, we assessed color morph flight initiation distance (FID), distance to the nearest refuge (DNR), and distance to chosen refuge (DR) in two populations of Aegean wall lizards from Naxos island. We also analyzed the type of refugia color morphs selected and their re-emergence behavior following a standardized intrusion event. We found that orange morphs have different escape behaviors from white and yellow morphs, and these differences are consistent in both of the populations we sampled. Orange morphs have shorter FIDs, DNRs, and DRs, select different refuge types, and re-emerge less often after an intruder event compared to white and yellow morphs. Observed differences in color morph escape behaviors support the idea that morphs have evolved alternative behavioral strategies that may play a role in population-level morph maintenance and loss.


2019 ◽  
Vol 50 (6) ◽  
pp. 2921-2930 ◽  
Author(s):  
Mauro Congiu ◽  
Massimo Trusel ◽  
Marco Pistis ◽  
Manuel Mameli ◽  
Salvatore Lecca

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Anita Burgos ◽  
Ken Honjo ◽  
Tomoko Ohyama ◽  
Cheng Sam Qian ◽  
Grace Ji-eun Shin ◽  
...  

Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscrew-like rolling behavior. We identified a population of interneurons in the nerve cord of Drosophila, termed Down-and-Back (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are required for robust escape responses to noxious stimuli. Electron microscopic circuit reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling command-like neurons. DnB activation promotes activity in Goro neurons, and coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact body bending motor responses. Thus, activity from nociceptors to DnB interneurons coordinates modular elements of nociceptive escape behavior.


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