Bacteria evoke alarm behaviour in zebrafish

Chia, Joanne Shu Ming; Wall, Elena S.; Wee, Caroline Lei; Rowland, Thomas A. J.; Cheng, Ruey‐Kuang; Cheow, Kathleen; Guillemin, Karen; Jesuthasan, Suresh

doi:10.1038/s41467-019-11608-9

Cited by 32 publications

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“…Previous reports indicated that at least two glomeruli 240 in the lateral and medial olfactory bulb regions respond to the alarm substance [19,37]. 241 Present results indicate that the glomerulus in the lateral bulb (LG) is innervated by 242 microvillous olfactory sensory neurons [15]. The LG cluster consists of 2 identifiable 243 large glomeruli, LG 3 and LG 4 from 3 dpf onwards in the classification proposed by 244 Braubach et.…”

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confidence: 72%

“…Supplementary Figure 5 Next, we examined the neural activity in the larvae. We first imaged the olfactory bulbs 137 of 5-7 day old Tg(gng8:GAL4, UAS:GCaMP6s) larvae where a small subset of olfactory 138 microvillus sensory neurons express GCaMP6s [44], and delivered Schreckstoff as 139 described previously [15,37]. A response to Schreckstoff was observed in the glomerular 140 termini of gng8-expressing neurons (Figure 2 A-C).…”

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confidence: 91%

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Neural correlates of state transitions elicited by a chemosensory danger cue

Jesuthasan

Krishnan

Cheng

et al. 2020

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Danger signals elicit an immediate behavioural response as well as a prolonged increase in sensitivity to threats. We investigated the alarm response in larval zebrafish to identify neural circuits underlying such transitions. 5-7 day old larvae react to the alarm substance (Schreckstoff ) by increased intervals between swim bouts and extended immobility. Calcium imaging indicates that olfactory sensory neurons innervating a lateral glomerulus detect the substance. Several telencephalic regions including the entopeduncular nucleus are also activated, with sustained activity outlasting stimulus delivery observable in the lateral habenula, posterior tuberculum, superior raphe, locus coeruleus, and periaqueductal gray. Consistent with the idea that these changes are related to an increased sensitivity to threats, larvae show increased dark avoidance after Schreckstoff removal. These results demonstrate that danger cues activate multiple brain circuits resulting in the expression of a continuum of defensive behaviors, some of which extend beyond stimulus detection. 4 system-wide changes to counter risk [1]. Regions of the vertebrate brain that process 5 and execute immediate responses, such as the freeze or the flight responses [23, 30], and 6 those mediating sustained responses [17, 56] have been identified in past studies [42].7Neuromodulators such as serotonin [12] and norepinephrine [26] have also been identified 8 as having critical roles. However, a whole-brain view of the neural dynamics when 9 transitions in central states [47] occur in an animal in response to a threat is lacking. 10Here, we explored the use of larval zebrafish, where in vivo brain-wide imaging of 11 neural activity can be conducted with relative ease [14,24], to examine neural circuits 12 1/15 and their dynamics during the transition in brain state in response to danger. As a 13 danger cue, we turned to alarm substances (or Schreckstoff ). These are released upon 14 physical injury to an individual and elicit a striking Schreckreaktion, or an alarm 15 response, in the entire shoal [16,25,36,48]. In general, the detection of such a cue results 16 in an immediate change in locomotion [28,49]. In zebrafish, in addition, other changes 17 such as an increase in anxiety-like behaviors remain even after the removal of the 18 cue [32,38], making it a good system to examine the steps in changes in central states. 19 Whether early zebrafish larvae (5-7 day old) ideally suited for whole-brain imaging 20show a Shreckreaktion has been debated. One study examined the ontogeny of the 21 response in zebrafish in detail by quantifying behavioral parameters associated with 22 45 Experimental methods 46 Are described in detail in extended supplementary data. 47 51 characterized and identified quantifiable parameters associated with normal swimming 52of 5-7 dpf larvae in this type of chamber over a period of 30 minutes. As described in 53 the past for larvae of an equivalent age [11], larvae swam in short bouts (Fig 1A, 1B). 54 Larvae explored the entire chamb...

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Neural correlates of state transitions elicited by a chemosensory danger cue

Jesuthasan

Krishnan

Cheng

et al. 2020

Preprint

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“…The recording was started within 30 s of fish being in the recording tanks. For exposure to Schreckstoff, fish were placed in 100 mL beakers containing 200 µL of heated skin extract (see (Chia et al, 2019) for extraction method) in 50 mL fish facility water for 2 minutes.…”

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confidence: 99%

The habenula clock influences prediction of danger

Basnakova

Cheng

Jcs

et al. 2020

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The lateral habenula, a regulator of neuromodulators that is activated by aversive stimuli, contains a molecular clock whose significance is unknown. Here, using zebrafish, we test the hypothesis that the habenula clock affects the switch in internal state that is triggered by an aversive stimulus. Consistent with the expression of clock genes, habenula neural activity varies in a circadian manner. Disruption of clock function, by expression of a truncated clock gene specifically in the habenula, did not affect acute responses to the alarm pheromone Schreckstoff. However, behaviours elicited by transient exposure to Schreckstoff namely freezing in a novel environment and dark avoidance, were reduced. Behaviours that are regulated by the pineal clock and not triggered by stressors were unaffected. These findings establish that the habenula clock independently influences the stress response induced by an aversive stimulus, indicating that this clock underlies circadian variation in response to a stressor.

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“…A growing number of studies have begun to address this gap in knowledge by characterizing the change in zebrafish swimming patterns in response to odors, identifying clear negative (avoidance) and positive (approach) chemotactic responses [4, 5, 7-12, 14, 15]. These studies investigated the behavioral responses to odors belonging to one or two of the following categories: food-related odors [7,8,21], social-related odors [9,13,29], decayrelated odors (polyamines in decomposing flesh) [30], and alarm odors [24,31,32]. This approach precludes the comparison of behavioral responses between all four odor categories within the same individual that is important to uncover stereotyped and odor-specific motor programs.…”

Section: Introductionmentioning

confidence: 99%

“…For example, to our knowledge, the response to aversive decay-related odors and alarm odors was not compared in the same individual. Moreover, odor-driven behaviors were either measured in groups of fish, thus masking potential inter-individual variability in odor sensitivity or preferences [9,13,21,24], or the interindividual variability was not quantified [7,8,[30][31][32][33]. Therefore, there is an important need for measuring and analyzing the behavioral responses of individual fish to a broad range of odors, spanning the natural stimulus space.…”

Section: Introductionmentioning

confidence: 99%

Stimulus-specific behavioral responses of zebrafish to a large range of odors exhibit individual variability

et al. 2020

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Background: Odor-driven behaviors such as feeding, mating, and predator avoidance are crucial for animal survival. The neural pathways processing these behaviors have been well characterized in a number of species, and involve the activity of diverse brain regions following stimulation of the olfactory bulb by specific odors. However, while the zebrafish olfactory circuitry is well understood, a comprehensive characterization linking odor-driven behaviors to specific odors is needed to better relate olfactory computations to animal responses. Results: Here, we used a medium-throughput setup to measure the swimming trajectories of 10 zebrafish in response to 17 ecologically relevant odors. By selecting appropriate locomotor metrics, we constructed ethograms systematically describing odor-induced changes in the swimming trajectory. We found that adult zebrafish reacted to most odorants using different behavioral programs and that a combination of a few relevant behavioral metrics enabled us to capture most of the variance in these innate odor responses. We observed that individual components of natural food and alarm odors do not elicit the full behavioral response. Finally, we show that zebrafish blood elicits prominent defensive behaviors similar to those evoked by skin extract and activates spatially overlapping olfactory bulb domains. Conclusion: Altogether, our results highlight a prominent intra-and inter-individual variability in zebrafish odordriven behaviors and identify a small set of waterborne odors that elicit robust responses. Our behavioral setup and our results will be useful resources for future studies interested in characterizing innate olfactory behaviors in aquatic animals.

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Bacteria evoke alarm behaviour in zebrafish

Cited by 32 publications

References 70 publications

Neural correlates of state transitions elicited by a chemosensory danger cue

Neural correlates of state transitions elicited by a chemosensory danger cue

The habenula clock influences prediction of danger

Stimulus-specific behavioral responses of zebrafish to a large range of odors exhibit individual variability

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