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Lovett-Barron, M.

Publications and source records attributed to Lovett-Barron, M..

6 recordsLinked to original sources

Relaxin-3 neurons of the zebrafish periaqueductal gray mediate behavioral responses evoked by darkness

Ambient illumination influences many aspects of brain function, including responses to threats. One brain region proposed to mediate these effects is the periaqueductal gray (PAG), an evolutionarily conserved midbrain structure that contains multiple subpopulations of peptidergic neurons. Here we ask which cell types in the larval zebrafish PAG respond to changes in ambient illumination. By registering post hoc gene expression to neurons recorded during exposure to sensory stimuli, we show that GABAergic PAG neurons expressing the neuropeptide Relaxin-3 (rln3a+) are persistently activated by darkness, while a neighboring subpopulation of GABAergic PAG neurons expressing penka is not. Zebrafish lacking rln3a show a reduction in locomotion during darkness. We propose that darkness recruits Relaxin-3-releasing PAG neurons to promote vigilance and potentiate defense circuits. These results identify a specific peptidergic population of PAG neurons that are potentially relevant to behavioral state dysregulation associated with excessive darkness.

neuroscience↗

Decay chemicals activate a pH-sensing pathway to initiate a persistent state

Animals use multiple sensory systems to identify signs of danger, including dead conspecifics. Fish can identify decaying conspecifics from chemosensory cues, which prompt a long-lasting avoidance; the neural basis of this persistent chemosensory-driven state is not understood. Here, we describe a persistent alarm state in larval zebrafish, where brief exposure to the polyamine decay product, cadaverine, initiates a minutes-long increase in heart rate and suppression of visually-evoked swimming. Cadaverine activates both olfactory and trigeminal neurons, with persistently-active cells in the forebrain and dorsolateral hindbrain. However, we find that cadaverine's persistent effects on hindbrain activity, heart rate, and locomotor suppression are not mediated by olfaction. Instead, they are mediated through trigeminal chemosensation of the basic pH of concentrated cadaverine in solution. Knockout of TrpA1 channels, which are expressed in trigeminal neurons and associated with chemical nociception across species, prevents the persistent suppression of movement from brief exposure to cadaverine. pH-responsive trigeminal neurons project into the dorsolateral hindbrain to mediate persistent activity and long-lasting locomotor suppression through local inhibition. These results demonstrate that non-olfactory chemosensation mediates persistent behavioral responses to death and decay in zebrafish, illustrating how diverse chemosensory systems detect ethologically-relevant cues to drive adaptive behavior.

neuroscience↗

Neuronal detection of social actions directs collective escape behavior

Animals in groups obtain information from their social partners to engage in collective behavior1-4. Social information transmission has been observed amongst individuals in fish schools5-8, bird flocks9,10, and human groups11,12, but the neural mechanisms for detecting socially transmitted information are poorly understood4,13-15. By studying the schooling glassfish Danionella cerebrum16-18, here we demonstrate that escape from danger is enhanced by visual perception of other escaping fish. We found that neural populations in the midbrain optic tectum19-21 and dorsal thalamus22,23 are activated by the rapid escape of social partners. These neurons are also driven by the sudden disappearance of virtual social partners, yet unaffected by disappearing stimuli without social relevance. Virtual fish schools that escape or disappear were sufficient to cause observers to escape, even in the absence of direct threats. These results demonstrate that rapid "social-off" detection in visual circuits enables the detection of socially transmitted threat information, which may be a particularly effective strategy for animals capable of rapid movement but limited visual range17,24. These results show how neural computations in individuals enables rapid information sharing in animal collectives4,15.

neuroscience↗

Development of neural circuits for social motion perception in schooling fish

Many animals move in groups, where collective behavior emerges from the interactions amongst individuals. These social interactions produce the coordinated movements of bird flocks and fish schools, but little is known about their developmental emergence and neurobiological foundations. By characterizing the visually-based schooling behavior of the micro glassfish Danionella cerebrum, here we found that social development progresses sequentially, with animals first acquiring the ability to aggregate, followed by postural alignment with social partners. This social maturation was accompanied by the development of neural populations in the midbrain and forebrain that were preferentially driven by visual stimuli that resemble the shape and movements of schooling fish. The development of these neural circuits enables the social coordination required for collective movement. One-Sentence SummaryThe collective behavior of schooling fish emerges with the development of neural populations selective to social motion.

neuroscience↗

Higher-order hub cells involved in feedforward motifs as critical factors in epileptic network instability

Neurological and psychiatric disorders are associated with pathological neural dynamics. The fundamental connectivity patterns of cell-cell communication networks that enable pathological dynamics to emerge remain unknown. We studied epileptic circuits using a newly developed integrated computational pipeline applied to cellular resolution functional imaging data. Control and preseizure neural dynamics in larval zebrafish and in chronically epileptic mice were captured using large-scale cellular-resolution calcium imaging. Biologically constrained effective connectivity modeling extracted the underlying cell-cell communication network. Novel analysis of the higher-order network structure revealed the existence of superhub cells that are unusually richly connected to the rest of the network through feedforward motifs. Instability in epileptic networks was causally linked to superhubs whose involvement in feedforward motifs critically enhanced downstream excitation. Disconnecting individual superhubs was significantly more effective in stabilizing epileptic networks compared to disconnecting hub cells defined traditionally by connection count. Collectively, these results predict a new, maximally selective and minimally invasive cellular target for seizure control. HighlightsO_LIHigher-order connectivity patterns of large-scale neuronal communication networks were studied in zebrafish and mice C_LIO_LIControl and epileptic networks were modeled from in vivo cellular resolution calcium imaging data C_LIO_LIRare superhub cells unusually richly connected to the rest of the network through higher-order feedforward motifs were identified C_LIO_LIDisconnecting single superhub neurons more effectively stabilized epileptic networks than targeting conventional hub cells defined by high connection count. C_LIO_LIThese data predict a maximally selective novel single cell target for minimally invasive seizure control C_LI

neuroscience↗

Multiple overlapping hypothalamus-brainstem circuits drive rapid threat avoidance

Animals survive environmental challenges by adapting their physiology and behavior through homeostatic regulatory processes, mediated in part by specific neuropeptide release from the hypothalamus. Animals can also avoid environmental stressors within seconds, a fast behavioral adaptation for which hypothalamic involvement is not established. Using brain-wide neural activity imaging in behaving zebrafish, here we find that hypothalamic neurons are rapidly engaged during common avoidance responses elicited by various environmental stressors. By developing methods to register cellular-resolution neural dynamics to multiplexed in situ gene expression, we find that each category of stressor recruits similar combinations of multiple peptidergic cell types in the hypothalamus. Anatomical analysis and functional manipulations demonstrate that these diverse cell types play shared roles in behavior, are glutamatergic, and converge upon spinal-projecting brainstem neurons required for avoidance. These data demonstrate that hypothalamic neural populations, classically associated with slow and specific homeostatic adaptations, also together give rise to fast and generalized avoidance behavior.

neuroscience↗