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Nature Jun 2018Escaping from imminent danger is an instinctive behaviour that is fundamental for survival, and requires the classification of sensory stimuli as harmless or...
Escaping from imminent danger is an instinctive behaviour that is fundamental for survival, and requires the classification of sensory stimuli as harmless or threatening. The absence of threat enables animals to forage for essential resources, but as the level of threat and potential for harm increases, they have to decide whether or not to seek safety . Despite previous work on instinctive defensive behaviours in rodents, little is known about how the brain computes the threat level for initiating escape. Here we show that the probability and vigour of escape in mice scale with the saliency of innate threats, and are well described by a model that computes the distance between the threat level and an escape threshold. Calcium imaging and optogenetics in the midbrain of freely behaving mice show that the activity of excitatory neurons in the deep layers of the medial superior colliculus (mSC) represents the saliency of the threat stimulus and is predictive of escape, whereas glutamatergic neurons of the dorsal periaqueductal grey (dPAG) encode exclusively the choice to escape and control escape vigour. We demonstrate a feed-forward monosynaptic excitatory connection from mSC to dPAG neurons, which is weak and unreliable-yet required for escape behaviour-and provides a synaptic threshold for dPAG activation and the initiation of escape. This threshold can be overcome by high mSC network activity because of short-term synaptic facilitation and recurrent excitation within the mSC, which amplifies and sustains synaptic drive to the dPAG. Therefore, dPAG glutamatergic neurons compute escape decisions and escape vigour using a synaptic mechanism to threshold threat information received from the mSC, and provide a biophysical model of how the brain performs a critical behavioural computation.
Topics: Animals; Calcium; Decision Making; Escape Reaction; Female; Male; Mice; Mice, Inbred C57BL; Models, Neurological; Neural Pathways; Optogenetics; Periaqueductal Gray; Superior Colliculi; Synapses
PubMed: 29925954
DOI: 10.1038/s41586-018-0244-6 -
Neuron Jun 2020The lateral parabrachial nucleus (lPBN) is a major target of spinal projection neurons conveying nociceptive input into supraspinal structures. However, the functional...
The lateral parabrachial nucleus (lPBN) is a major target of spinal projection neurons conveying nociceptive input into supraspinal structures. However, the functional role of distinct lPBN efferents in diverse nocifensive responses have remained largely uncharacterized. Here we show that that the lPBN is required for escape behaviors and aversive learning to noxious stimulation. In addition, we find that two populations of efferent neurons from different regions of the lPBN collateralize to distinct targets. Activation of efferent projections to the ventromedial hypothalamus (VMH) or lateral periaqueductal gray (lPAG) drives escape behaviors, whereas activation of lPBN efferents to the bed nucleus stria terminalis (BNST) or central amygdala (CEA) generates an aversive memory. Finally, we provide evidence that dynorphin-expressing neurons, which span cytoarchitecturally distinct domains of the lPBN, are required for aversive learning.
Topics: Animals; Avoidance Learning; Central Amygdaloid Nucleus; Escape Reaction; Mice; Neural Pathways; Neurons, Efferent; Nociception; Optogenetics; Pain; Parabrachial Nucleus; Periaqueductal Gray; Septal Nuclei; Ventromedial Hypothalamic Nucleus
PubMed: 32289251
DOI: 10.1016/j.neuron.2020.03.014 -
Nature Jan 2023When faced with predatory threats, escape towards shelter is an adaptive action that offers long-term protection against the attacker. Animals rely on knowledge of safe...
When faced with predatory threats, escape towards shelter is an adaptive action that offers long-term protection against the attacker. Animals rely on knowledge of safe locations in the environment to instinctively execute rapid shelter-directed escape actions. Although previous work has identified neural mechanisms of escape initiation, it is not known how the escape circuit incorporates spatial information to execute rapid flights along the most efficient route to shelter. Here we show that the mouse retrosplenial cortex (RSP) and superior colliculus (SC) form a circuit that encodes the shelter-direction vector and is specifically required for accurately orienting to shelter during escape. Shelter direction is encoded in RSP and SC neurons in egocentric coordinates and SC shelter-direction tuning depends on RSP activity. Inactivation of the RSP-SC pathway disrupts the orientation to shelter and causes escapes away from the optimal shelter-directed route, but does not lead to generic deficits in orientation or spatial navigation. We find that the RSP and SC are monosynaptically connected and form a feedforward lateral inhibition microcircuit that strongly drives the inhibitory collicular network because of higher RSP input convergence and synaptic integration efficiency in inhibitory SC neurons. This results in broad shelter-direction tuning in inhibitory SC neurons and sharply tuned excitatory SC neurons. These findings are recapitulated by a biologically constrained spiking network model in which RSP input to the local SC recurrent ring architecture generates a circular shelter-direction map. We propose that this RSP-SC circuit might be specialized for generating collicular representations of memorized spatial goals that are readily accessible to the motor system during escape, or more broadly, during navigation when the goal must be reached as fast as possible.
Topics: Animals; Mice; Escape Reaction; Neural Pathways; Neurons; Predatory Behavior; Spatial Memory; Spatial Navigation; Superior Colliculi; Gyrus Cinguli; Time Factors; Goals
PubMed: 36544025
DOI: 10.1038/s41586-022-05553-9 -
Current Biology : CB Sep 2018Carlson and colleagues introduce mobbing an anti-predator behaviour found in many animals.
Carlson and colleagues introduce mobbing an anti-predator behaviour found in many animals.
Topics: Animals; Cooperative Behavior; Escape Reaction; Predatory Behavior; Social Behavior; Vocalization, Animal
PubMed: 30253143
DOI: 10.1016/j.cub.2018.06.025 -
Psychophysiology Jun 2017This research examined human defensive reactivity when exposure to an aversive event could be escaped but not entirely avoided. Prolonged visual cues indicated whether...
This research examined human defensive reactivity when exposure to an aversive event could be escaped but not entirely avoided. Prolonged visual cues indicated whether exposure to an upcoming aversive (i.e., disgusting) picture could be terminated after onset (escaped) or not, or that a neutral go signal would appear. Acoustically elicited startle reflexes were measured during each cue interval, as were cardiac and skin conductance activity. Early in the cuing interval, startle reflexes were potentiated during both escape and inescapable exposure trials, compared to the simple motor context. Later in the interval, reflexes remained potentiated for both escapable and inescapable trials, with potentiation further enhanced when aversive exposure could not be escaped compared to when exposure could be escaped. Heart rate deceleration in the cuing interval indicated increased vigilance when preparing any (escape or neutral) action, whereas skin conductance responding indicated enhanced sympathetic action mobilization particularly in an escape context. These data suggest that startle reflexes engaged in an escape context reflect both motor-related response inhibition and aversive potentiation, and they indicate that defensive motivation is engaged whenever aversive exposure is guaranteed, regardless of whether it can be escaped or not.
Topics: Adolescent; Arousal; Autonomic Nervous System; Blood Pressure; Emotions; Escape Reaction; Fear; Female; Galvanic Skin Response; Heart Rate; Humans; Male; Reflex, Startle; Young Adult
PubMed: 28218794
DOI: 10.1111/psyp.12842 -
Proceedings of the National Academy of... Mar 2020Insect nervous systems offer unique advantages for studying interactions between sensory systems and behavior, given their complexity with high tractability. By...
Insect nervous systems offer unique advantages for studying interactions between sensory systems and behavior, given their complexity with high tractability. By examining the neural coding of salient environmental stimuli and resulting behavioral output in the context of environmental stressors, we gain an understanding of the effects of these stressors on brain and behavior and provide insight into normal function. The implication of neonicotinoid (neonic) pesticides in contributing to declines of nontarget species, such as bees, has motivated the development of new compounds that can potentially mitigate putative resistance in target species and declines of nontarget species. We used a neuroethologic approach, including behavioral assays and multineuronal recording techniques, to investigate effects of imidacloprid (IMD) and the novel insecticide sulfoxaflor (SFX) on visual motion-detection circuits and related escape behavior in the tractable locust system. Despite similar LD values, IMD and SFX evoked different behavioral and physiological effects. IMD significantly attenuated collision avoidance behaviors and impaired responses of neural populations, including decreases in spontaneous firing and neural habituation. In contrast, SFX displayed no effect at a comparable sublethal dose. These results show that neonics affect population responses and habituation of a visual motion detection system. We propose that differences in the sublethal effects of SFX reflect a different mode of action than that of IMD. More broadly, we suggest that neuroethologic assays for comparative neurotoxicology are valuable tools for fully addressing current issues regarding the proximal effects of environmental toxicity in nontarget species.
Topics: Animals; Environmental Exposure; Escape Reaction; Habituation, Psychophysiologic; Insecticides; Lethal Dose 50; Locusta migratoria; Motion; Motor Neurons; Neonicotinoids; Nitro Compounds; Pyridines; Sulfur Compounds
PubMed: 32094166
DOI: 10.1073/pnas.1916432117 -
Current Biology : CB Jul 2022In many instances, external sensory-evoked neuronal activity is used by the brain to select the most appropriate behavioral response. Predator-avoidance behaviors such...
In many instances, external sensory-evoked neuronal activity is used by the brain to select the most appropriate behavioral response. Predator-avoidance behaviors such as freezing and escape are of particular interest since these stimulus-evoked responses are behavioral manifestations of a decision-making process that is fundamental to survival. Over the lifespan of an individual, however, the threat value of agents in the environment is believed to undergo constant revision, and in some cases, repeated avoidance of certain stimuli may no longer be an optimal behavioral strategy. To begin to study this type of adaptive control of decision-making, we devised an experimental paradigm to probe the properties of threat escape in the laboratory mouse Mus musculus. First, we found that while robust escape to visual looming stimuli can be observed after 2 days of social isolation, mice can also rapidly learn that such stimuli are non-threatening. This learned suppression of escape (LSE) is extremely robust and can persist for weeks and is not a generalized adaptation, since flight responses to novel live prey and auditory threat stimuli in the same environmental context were maintained. We also show that LSE cannot be explained by trial number or a simple form of stimulus desensitization since it is dependent on threat-escape history. We propose that the action selection process mediating escape behavior is constantly updated by recent threat history and that LSE can be used as a robust model system to understand the neurophysiological mechanisms underlying experience-dependent decision-making.
Topics: Animals; Avoidance Learning; Brain; Escape Reaction; Mice
PubMed: 35659863
DOI: 10.1016/j.cub.2022.05.022 -
Current Opinion in Neurobiology Apr 2012Escape behaviors are crucial to survive predator encounters. Touch to the head of Caenorhabditis elegans induces an escape response where the animal rapidly backs away... (Review)
Review
Escape behaviors are crucial to survive predator encounters. Touch to the head of Caenorhabditis elegans induces an escape response where the animal rapidly backs away from the stimulus and suppresses foraging head movements. The coordination of head and body movements facilitates escape from predacious fungi that cohabitate with nematodes in organic debris. An appreciation of the natural habitat of laboratory organisms, like C. elegans, enables a comprehensive neuroethological analysis of behavior. In this review we discuss the neuronal mechanisms and the ecological significance of the C. elegans touch response.
Topics: Animals; Caenorhabditis elegans; Escape Reaction; Ethology; Neural Pathways; Neurology
PubMed: 22226513
DOI: 10.1016/j.conb.2011.12.007 -
Current Biology : CB Jan 2015
Topics: Adaptation, Biological; Animals; Escape Reaction; Invertebrates; Vertebrates; Vision, Ocular
PubMed: 25602301
DOI: 10.1016/j.cub.2014.11.011 -
PLoS Computational Biology Jan 2022Bird flocks under predation demonstrate complex patterns of collective escape. These patterns may emerge by self-organization from local interactions among...
Bird flocks under predation demonstrate complex patterns of collective escape. These patterns may emerge by self-organization from local interactions among group-members. Computational models have been shown to be valuable for identifying what behavioral rules may govern such interactions among individuals during collective motion. However, our knowledge of such rules for collective escape is limited by the lack of quantitative data on bird flocks under predation in the field. In the present study, we analyze the first GPS trajectories of pigeons in airborne flocks attacked by a robotic falcon in order to build a species-specific model of collective escape. We use our model to examine a recently identified distance-dependent pattern of collective behavior: the closer the prey is to the predator, the higher the frequency with which flock members turn away from it. We first extract from the empirical data of pigeon flocks the characteristics of their shape and internal structure (bearing angle and distance to nearest neighbors). Combining these with information on their coordination from the literature, we build an agent-based model adjusted to pigeons' collective escape. We show that the pattern of turning away from the predator with increased frequency when the predator is closer arises without prey prioritizing escape when the predator is near. Instead, it emerges through self-organization from a behavioral rule to avoid the predator independently of their distance to it. During this self-organization process, we show how flock members increase their consensus over which direction to escape and turn collectively as the predator gets closer. Our results suggest that coordination among flock members, combined with simple escape rules, reduces the cognitive costs of tracking the predator while flocking. Such escape rules that are independent of the distance to the predator can now be investigated in other species. Our study showcases the important role of computational models in the interpretation of empirical findings of collective behavior.
Topics: Animals; Columbidae; Computational Biology; Computer Simulation; Escape Reaction; Mass Behavior; Species Specificity
PubMed: 35007287
DOI: 10.1371/journal.pcbi.1009772