scholarly journals Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Anita Burgos ◽  
Ken Honjo ◽  
Tomoko Ohyama ◽  
Cheng Sam Qian ◽  
Grace Ji-eun Shin ◽  
...  
Keyword(s):  
Escape Behavior ◽  
Nociceptive Behavior ◽  
Electron Microscopic ◽  
Noxious Heat ◽  
Sensory Stimuli ◽  
Motor Pathways ◽  
Motor Circuits ◽  
Drosophila Larvae ◽  
Noxious Stimuli ◽  
Escape Behaviors

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.

The Neural Basis of Escape Behavior in Vertebrates

2020 ◽  
Vol 43 (1) ◽  
pp. 417-439 ◽  
Author(s):  
Tiago Branco ◽  
Peter Redgrave
Keyword(s):  
Neural Circuits ◽  
Escape Behavior ◽  
Building Blocks ◽  
Normative Theory ◽  
Neural Systems ◽  
Adaptive Behaviors ◽  
Neural Basis ◽  
Sensory Stimuli ◽  
Evolutionarily Conserved ◽  
Escape Behaviors

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.

scholarly journals A core signaling mechanism at the origin of animal nociception

2017 ◽  
Author(s):  
Oscar M. Arenas ◽  
Emanuela E. Zaharieva ◽  
Alessia Para ◽  
Constanza Vásquez-Doorman ◽  
Christian P. Petersen ◽  
...  
Keyword(s):  
Heat Exposure ◽  
Oxygen Species ◽  
Common Ancestry ◽  
Protective Behavior ◽  
Noxious Heat ◽  
Signaling Mechanism ◽  
Early Markers ◽  
Core Function ◽  
Noxious Stimuli ◽  
Escape Behaviors

All animals must detect noxious stimuli to initiate protective behavior, but the evolutionary origin of nociceptive systems is not well understood. Here, we show that a remarkably conserved signaling mechanism mediates the detection of noxious stimuli in animals as diverse as flatworms and humans. Planarian flatworms are amongst the simplest bilateral animals with a centralized nervous system, and capable of directed behavior. We demonstrate that noxious heat and irritant chemicals elicit robust escape behaviors in the planarian Schmidtea mediterranea, and that the conserved ion channel TRPA1 is required for these responses. TRPA1 mutant fruit flies (Drosophila) are also defective in the avoidance of noxious heat 1-3. Unexpectedly, we find that either the planarian or the human TRPA1 can restore noxious heat avoidance to TRPA1 mutant Drosophila, even though neither is directly activated by heat. Instead, our data suggest that TRPA1 activation is mediated by H2O2/Reactive Oxygen Species, early markers of tissue damage rapidly produced as a result of heat exposure. Together, our data reveal a core function for TRPA1 in noxious heat transduction, demonstrate its conservation from planarians to humans, and imply that human nociceptive systems may share a common ancestry with those of most extant animals, tracing back their origin to a progenitor that lived more than 500 million years ago.

scholarly journals Pharmacological or genetic targeting of Transient Receptor Potential (TRP) channels can disrupt the planarian escape response

2019 ◽  
Author(s):  
Ziad Sabry ◽  
Alicia Ho ◽  
Danielle Ireland ◽  
Christina Rabeler ◽  
Olivier Cochet-Escartin ◽  
...  
Keyword(s):  
Transient Receptor Potential ◽  
Trp Channels ◽  
Escape Behavior ◽  
Receptor Potential ◽  
Allyl Isothiocyanate ◽  
Noxious Heat ◽  
Dugesia Japonica ◽  
Noxious Stimuli ◽  
Transient Receptor ◽  
Genetic Targeting

AbstractIn response to noxious stimuli, planarians cease their typical ciliary gliding and exhibit an oscillatory type of locomotion called scrunching. We have previously characterized the biomechanics of scrunching and shown that it is induced by specific stimuli, such as amputation, noxious heat, and extreme pH. Because these specific inducers are known to activate Transient Receptor Potential (TRP) channels in other systems, we hypothesized that TRP channels control scrunching. We found that chemicals known to activate TRPA1 (allyl isothiocyanate (AITC) and hydrogen peroxide) and TRPV (capsaicin and anandamide) in other systems induce scrunching in the planarian species Dugesia japonica and, except for anandamide, in Schmidtea mediterranea. To confirm that these responses were specific to either TRPA1 or TRPV, respectively, we tried to block scrunching using selective TRPA1 or TRPV antagonists and RNA interference (RNAi) mediated knockdown. Unexpectedly, co-treatment with a mammalian TRPA1 antagonist, HC-030031, enhanced AITC-induced scrunching by decreasing the latency time, suggesting an agonistic relationship in planarians. We further confirmed that TRPA1 in both species is necessary for AITC-induced scrunching using RNAi. Conversely, while co-treatment of a mammalian TRPV antagonist, SB-366791, also enhanced capsaicin-induced reactions in D. japonica, combined knockdown of two previously identified D. japonica TRPV genes (DjTRPVa and DjTRPVb) did not inhibit capsaicin-induced scrunching. Surprisingly, RNAi of either DjTRPAa or DjTRPVa/DjTRPVb disrupted scrunching induced by the endocannabinoid and TRPV agonist, anandamide. Overall, our results show that although scrunching induction can involve different initial pathways for sensing stimuli, this behavior’s signature dynamical features are independent of the inducer, implying that scrunching is a stereotypical planarian escape behavior in response to various noxious stimuli that converge on a single downstream pathway. Understanding which aspects of nociception are conserved or not across different organisms can provide insight into the underlying regulatory mechanisms to better understand pain sensation.

scholarly journals Formin3 directs dendritic architecture via microtubule regulation and is required for somatosensory nociceptive behavior

Development ◽  
2021 ◽  
Author(s):  
Ravi Das ◽  
Shatabdi Bhattacharjee ◽  
Jamin M. Letcher ◽  
Jenna M. Harris ◽  
Sumit Nanda ◽  
...  
Keyword(s):  
Sensory Neurons ◽  
Time Course ◽  
Neuronal Function ◽  
Nociceptive Behavior ◽  
Noxious Heat ◽  
Cytoskeletal Organization ◽  
Nociceptive Neurons ◽  
Charcot Marie Tooth ◽  
Drosophila Larvae ◽  
Severe Impairment

Dendrite shape impacts functional connectivity and is mediated by organization and dynamics of cytoskeletal fibers. Identifying molecular factors that regulate dendritic cytoskeletal architecture is therefore important in understanding mechanistic links between cytoskeletal organization and neuronal function. We identified Formin3 (Form3) as a critical regulator of cytoskeletal architecture in nociceptive sensory neurons in Drosophila larvae. Time course analyses reveal Form3 is cell-autonomously required to promote dendritic arbor complexity. We show that form3 is required for the maintenance of a population of stable dendritic microtubules (MTs), and mutants exhibit defects in the localization of dendritic mitochondria, satellite Golgi, and the TRPA channel Painless. Form3 directly interacts with MTs via FH1-FH2 domains. Mutations in human Inverted Formin 2 (INF2; ortholog of form3) have been causally linked to Charcot-Marie-Tooth (CMT) disease. CMT sensory neuropathies lead to impaired peripheral sensitivity. Defects in form3 function in nociceptive neurons result in severe impairment of noxious heat-evoked behaviors. Expression of the INF2 FH1-FH2 domains partially recovers form3 defects in MTs and nocifensive behavior, suggesting conserved functions, thereby providing putative mechanistic insights into potential etiologies of CMT sensory neuropathies.

scholarly journals Action selection based on multiple-stimulus aspects in the wind-elicited escape behavior of crickets

2021 ◽  
Author(s):  
Nodoka Sato ◽  
Hisashi Shidara ◽  
Hiroto Ogawa
Keyword(s):  
Escape Behavior ◽  
Movement Direction ◽  
Neural Basis ◽  
Stimulus Velocity ◽  
Sensory Stimuli ◽  
Defensive Behaviors ◽  
Multiple Stimulus ◽  
Stimulus Parameters ◽  
Direction Control ◽  
Escape Responses

ABSTRACTAnimals detect approaching predators via sensory inputs through various modalities and immediately show an appropriate behavioral response to survive. Escape behavior is essential to avoid the predator’s attack and is more frequently observed than other defensive behaviors. In some species, multiple escape responses are exhibited with different movements. It has been reported that the approaching speed of a predator is important in choosing which escape action to take among the multiple responses. However, it is unknown whether other aspects of sensory stimuli, that indicate the predator’s approach, affect the selection of escape responses. We focused on two distinct escape responses (running and jumping) to a stimulus (short airflow) in crickets and examined the effects of multiple stimulus aspects (including the angle, velocity, and duration) on the choice between these escape responses. We found that the faster and longer the airflow, the more frequently the crickets jumped, meaning that they could choose their escape response depending on both velocity and duration of the stimulus. This result suggests that the neural basis for choosing escape responses includes the integration process of multiple stimulus parameters. It was also found that the moving speed and distance changed depending on the stimulus velocity and duration during running but not during jumping, suggesting higher adaptability of the running escape. In contrast, the movement direction was accurately controlled regardless of the stimulus parameters in both responses. The escape direction depended only on stimulus orientation, but not on velocity and duration.Summary statementWhen air currents triggering escape are faster and longer, crickets more frequently jump than run. Running speed and distance depend on stimulus velocity and duration, but direction control is independent.

scholarly journals Discrete escape responses are generated by neuropeptide-mediated circuit logic

2020 ◽  
Author(s):  
Bibi Nusreen Imambocus ◽  
Annika Wittich ◽  
Federico Tenedini ◽  
Fangmin Zhou ◽  
Chun Hu ◽  
...  
Keyword(s):  
Escape Behavior ◽  
Sensory Information ◽  
Environmental Threats ◽  
Order Processing ◽  
Relaxin Family ◽  
Escape Responses ◽  
Discrete Domains ◽  
Light Avoidance ◽  
Escape Behaviors ◽  
Selection Of

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.

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 ◽  
...  
Keyword(s):  
Animal Species ◽  
Escape Behavior ◽  
Negative Events ◽  
Innate Response ◽  
Lateral Habenula ◽  
Aversive Stimuli ◽  
External Threats ◽  
Glutamatergic Signaling ◽  
Excitatory Projection ◽  
Escape Behaviors

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.

1802 Effects of aging on escape behavior and c-fos expression following noxious heat stimulation to the hind paw in rats

1997 ◽  
Vol 28 ◽  
pp. S217
Author(s):  
Koichi Iwata ◽  
Yoshiyuki Tsuboi ◽  
Kaori Kitajima ◽  
Emi Nomoto ◽  
Kenro Kanda ◽  
...  
Keyword(s):  
Escape Behavior ◽  
Noxious Heat ◽  
Heat Stimulation ◽  
Fos Expression ◽  
Effects Of Aging

scholarly journals Author response: Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

2018 ◽  
Author(s):  
Anita Burgos ◽  
Ken Honjo ◽  
Tomoko Ohyama ◽  
Cheng Sam Qian ◽  
Grace Ji-eun Shin ◽  
...  
Keyword(s):  
Escape Behavior ◽  
Author Response ◽  
Motor Pathways

scholarly journals Rapid spatial learning controls instinctive defensive behavior in mice

2017 ◽  
Author(s):  
Ruben Vale ◽  
Dominic A. Evans ◽  
Tiago Branco
Keyword(s):  
Defensive Behavior ◽  
Escape Behavior ◽  
Food Sources ◽  
Defensive Strategy ◽  
Sensory Stimuli ◽  
Defensive Behaviors ◽  
Spatial Environment ◽  
Defensive Action ◽  
Access To Food ◽  
Innate Behaviors

SummaryInstinctive defensive behaviors are essential for animal survival. Across the animal kingdom there are sensory stimuli that innately represent threat and trigger stereotyped behaviors such as escape or freezing [1-4]. While innate behaviors are considered to be hard-wired stimulus-responses [5], they act within dynamic environments, and factors such as the properties of the threat [6-9] and its perceived intensity [1, 10, 11], access to food sources [12-14] or expectations from past experience [15, 16], have been shown to influence defensive behaviors, suggesting that their expression can be modulated. However, despite recent work [2, 4, 17-21], little is known about how flexible mouse innate defensive behaviors are, and how quickly they can be modified by experience. To address this, we have investigated the dependence of escape behavior on learned knowledge about the spatial environment, and how the behavior is updated when the environment changes acutely. Using behavioral assays with innately threatening visual and auditory stimuli, we show that the primary goal of escape in mice is to reach a previously memorized shelter location. Memory of the escape target can be formed in a single shelter visit lasting less than 20 seconds, and changes in the spatial environment lead to a rapid update of the defensive action, including changing the defensive strategy from escape to freezing. Our results show that while there are innate links between specific sensory features and defensive behavior, instinctive defensive actions are surprisingly flexible and can be rapidly updated by experience to adapt to changing spatial environments.

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