A bidirectional network for appetite control in larval zebrafish

Wee, Caroline Lei; Song, Erin; Johnson, Robert E.; Ailani, Deepak; Randlett, Owen; Kim, Ji-Yoon; Nikitchenko, Maxim; Bahl, Armin; Yang, Chao-Tsung; Ahrens, Misha B.; Kawakami, Koichi; Engert, Florian; Kunes, Sam

doi:10.7554/elife.43775

Cited by 66 publications

(62 citation statements)

References 72 publications

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“…The OXT circuit modulates nocifensive behavior via brainstem premotor neurons 6 . Since it projects extensively into other parts of the hypothalamus, as well as the pituitary gland, these downstream regions may be involved in mediating its effects appetite 25 .…”

Section: Resultsmentioning

confidence: 99%

“…In mammals, social isolation is associated not only with increases in aversive behavior, but also with a reduction in positive-valence behaviors such as feeding 22 . To determine if this is also the case in larval zebrafish, we first made use of an established and quantitative food intake assay that measures gut fluorescence intensity caused by the ingestion of fluorescently-labeled paramecia 23–25 (Fig. 4a).…”

Section: Resultsmentioning

confidence: 99%

“…4a). In this assay, larval fish were food deprived for a period of two hours to increase appetite 23–25 , either in isolation or in the presence of conspecific fish (Fig. 4a).…”

Section: Resultsmentioning

confidence: 99%

“…For experiments in which feeding was assessed, larvae that had been continuously fed with an excess of paramecia from 5 dpf were either isolated or placed in groups of 3, in 35 mm dishes (3 ml embryo water), in the absence of food . After 2 hours, fluorescent-labeled paramecia was added followed by a quick fixation after 30 min (full protocol is described in Wee et al, eLife , 2019 25 ). Sensory cues were generated and presented as described above for pERK experiments.…”

Section: Methodsmentioning

confidence: 99%

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Social isolation modulates appetite and defensive behavior via a common oxytocinergic circuit in larval zebrafish

Wee

Song²,

Nikitchenko

et al. 2020

Preprint

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24How brains encode social stimuli and transform these representations into advantageous 25 behavioral responses is not well-understood. Here, we show that social isolation activates an 26 oxytocinergic, nociceptive circuit in the larval zebrafish hypothalamus. We further demonstrate 27 that chemical cues released from conspecific animals modulate its activity to regulate defensive 28 behaviors and appetite. Our collective data reveals a model through which social stimuli can be 29 integrated into fundamental neural circuits to mediate adaptive behaviour. 30 31 32 33 34In mammals, signaling in oxytocinergic (OXT) circuits modulates a wide spectrum of socially 36 driven behaviors, ranging from pair bonding and parental care to the responses to stress and 37 pain 1-3 . OXT has also been described as a potent regulator of appetite 4,5 . We reported recently 38 that the larval zebrafish OXT circuit encodes a response to aversive, particularly noxious stimuli 39 and directly drives nocifensive behavior via brainstem premotor targets 6 . Moreover, studies in 40 both zebrafish 6-8 and mammals 9,10 suggest that the OXT-expressing neuronal population is 41 anatomically and functionally diverse, and might also modulate multiple behaviors in zebrafish. 42Here, in a brain-wide screen 11 for neuronal populations whose activity reflects social context, we 43show that larval zebrafish oxytocinergic circuits display diverse responses to conspecific 44 chemosensory stimuli, and are key effectors for social context modulation of nociceptive and 45 appetite-driven behaviors. Our results reveal a simple algorithm by which neuromodulatory 46 neurons can represent social context to exert flexible control over hard-wired behavioral drives. 47 48 RESULTS 49Brain-wide activity mapping of social isolation and its rescue by conspecific chemical cues 50Using pERK based whole-brain activity mapping (MAP-Mapping 11 ), neural activity in brains of 51 briefly (2 hrs) socially-isolated larvae (7 -8 days-post-fertilization; dpf) was compared to 52 animals that had been maintained in the presence of similarly-aged conspecifics. We found that 53 isolated fish showed an enhancement of neural activity in specific regions, including the 54 telencephalon (especially subpallium), hindbrain, locus coeruleus, area postrema, caudal 55 hypothalamus, preoptic area (PO, homolog of the hypothalamic paraventricular nucleus in 56 mammals) and posterior tuberculum (PT) ( Fig. 1a-b , Supplementary Movie 1, Supplementary 57Data 1). Many of these same regions are activated by noxious or aversive stimuli 6,7 ; they may 58 thus represent the signature activity pattern of a negative internal state, which can be similarly 59 triggered by social deprivation. Neurons expressing the peptide oxytocin (OXT) are abundant in 60 the PO and PT 6,12,13 regions, and as we describe below, OXT-positive neuron clusters in both of 61 these areas (OXT PO and OXT PT respectively) display greater activity in socially-isolated fish. To 62 acquire a more precise quantitation of OXT activi...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

“…4a). In this assay, larval fish were food deprived for a period of two hours to increase appetite 23–25 , either in isolation or in the presence of conspecific fish (Fig. 4a).…”

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Social isolation modulates appetite and defensive behavior via a common oxytocinergic circuit in larval zebrafish

Wee

Song²,

Nikitchenko

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The authors showed that food‐deprived larvae had active neurons at the caudal hypothalamus (CH), but inactive ones in the lateral hypothalamus (LH). This was reversed during meals when neuronal activity switches “off” at CH and “on” at LH (Wee et al, 2019). The transgenic zebrafish lines used in that study (Wee et al, 2019) do not exist in Astyanax CF.…”

Section: Subterranean Life With Scarce Foodmentioning

confidence: 99%

Subterranean life: Behavior, metabolic, and some other adaptations of Astyanax cavefish

et al. 2020

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The ability of fishes to adapt to any aquatic environment seems limitless. It is enthralling how new species keep appearing at the deep sea or in subterranean environments. There are close to 230 known species of cavefishes, still today the best-known cavefish is Astyanax mexicanus, a Characid that has become a model organism, and has been studied and scrutinized since 1936. There are two morphotypes for A. mexicanus, a surface fish and a cavefish. The surface fish lives in central and northeastern Mexico and south of the United States, while the cavefish is endemic to the "Sierra del Abra-Tanchipa region" in northeast Mexico. The extensive genetic and genomic analysis depicts a complex origin for Astyanax cavefish, with multiple cave invasions and persistent gene flow among cave populations. The surface founder population prevails in the same region where the caves are. In this review, we focus on both morphotype's main morphological and physiological differences, but mainly in recent discoveries about behavioral and metabolic adaptations for subterranean life. These traits may not be as obvious as the troglomorphic characteristics, but are key to understand how Astyanax cavefish thrives in this environment of perpetual darkness.

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d‐Amphetamine and Feeding States Cohesively Affect Locomotion and Motor Neuron Response in Zebrafish Larvae

Bansal,

Roitman,

Jung

2024

Brain and Behavior

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PurposeAmphetamine (AMPH) increases locomotor activities in animals, and the locomotor response to AMPH is further modulated by caloric deficits such as food deprivation and restriction. The increment in locomotor activity regulated by AMPH‐caloric deficit concomitance can be further modulated by varying feeding schedules (e.g., acute and chronic food deprivation and acute feeding after chronic food deprivation). However, the effects of different feeding schedules on AMPH‐induced locomotor activity are yet to be explicated. Here, we have explored the stimulatory responses of acutely administered D‐amphetamine in locomotion under systematically varying feeding states (fed/sated and food deprivation) and schedules (chronic and acute) in zebrafish larvae.MethodWe exposed wild‐type and transgenic [Tg(mnx1:GCaMP5)] zebrafish larvae to 0.7 µM concentration of AMPH and measured swimming activity and spinal motor neuron activity in vivo in real time. The analysis involved time‐elapsed and cumulative manner pre‐ and post‐AMPH treatment in four different caloric states including acute and chronic schedules of feeding and hunger. Both locomotor and motor neuron activities were compared in all four states in both fish lines.FindingsOur results show that locomotion and motor neuron activity increased in both chronic and acute food deprivation post‐AMPH treatment cumulatively. A steady increase in locomotion was observed in acute food deprivation compared to an immediate abrupt increase in chronic food‐deprivation state. The ad libitum‐fed larvae exhibited a moderate increase both in locomotion and motor neuron activity. Conversely to all other caloric states, food‐sated (acute feeding after chronic food deprivation) larvae moved moderately less and exhibited a mild decrease in motor neuron activity after AMPH treatment.ConclusionThese results reveal the importance of cohesive effects of feeding schedule and AMPH treatment by revealing the changes in stimulatory characteristics of AMPH on locomotion and motor neuron activity in acute and chronic feeding states.

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A bidirectional network for appetite control in larval zebrafish

Cited by 66 publications

References 72 publications

Social isolation modulates appetite and defensive behavior via a common oxytocinergic circuit in larval zebrafish

Social isolation modulates appetite and defensive behavior via a common oxytocinergic circuit in larval zebrafish

Subterranean life: Behavior, metabolic, and some other adaptations of Astyanax cavefish

d‐Amphetamine and Feeding States Cohesively Affect Locomotion and Motor Neuron Response in Zebrafish Larvae

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