Neuromodulatory Regulation of Behavioral Individuality in Zebrafish

• Published in: Neuron (Cambridge, Mass.) Vol. 91; no. 3; pp. 587 - 601
• Main Authors: Pantoja, Carlos, Hoagland, Adam, Carroll, Elizabeth C., Karalis, Vasiliki, Conner, Alden, Isacoff, Ehud Y.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 03.08.2016; Elsevier Limited
• Subjects: Acoustic Stimulation; Animal behavior; Animals; Animals, Genetically Modified; Apomorphine - pharmacology; Danio rerio; Dorsal Raphe Nucleus - cytology; Dorsal Raphe Nucleus - drug effects; Dorsal Raphe Nucleus - metabolism; Dorsal Raphe Nucleus - physiology; Habituation, Psychophysiologic - drug effects; Habituation, Psychophysiologic - physiology; Individuality; Neurons; Quipazine - pharmacology; Reflex, Startle - drug effects; Reflex, Startle - physiology; Rhodopsin - biosynthesis; Rhodopsin - genetics; Serotonergic Neurons - drug effects; Serotonergic Neurons - metabolism; Serotonergic Neurons - physiology; Serotonin; Serotonin - metabolism; Zebrafish; Zebrafish - physiology
• DOI: 10.1016/j.neuron.2016.06.016
• ISSN: 0896-6273

Inter-individual behavioral variation is thought to increase fitness and aid adaptation to environmental change, but the underlying mechanisms are poorly understood. We find that variation between individuals in neuromodulatory input contributes to individuality in short-term habituation of the zebrafish (Danio Rerio) acoustic startle response (ASR). ASR habituation varies greatly between individuals, but differences are stable over days and are heritable. Acoustic stimuli that activate ASR-command Mauthner cells also activate dorsal raphe nucleus (DRN) serotonergic neurons, which project to the vicinity of the Mauthner cells and their inputs. DRN neuron activity decreases during habituation in proportion to habituation and a genetic manipulation that reduces serotonin content in DRN neurons increases habituation, whereas serotonergic agonism or DRN activation with ChR2 reduces habituation. Finally, level of rundown of DRN activity co-segregates with extent of behavioral habituation across generations. Thus, variation between individuals in neuromodulatory input contributes to individuality in a core adaptive behavior. [Display omitted] •Acoustic startle response (ASR) habituation varies widely among individual zebrafish•Acoustic stimuli activate dorsal raphe nucleus (DRN), which projects to the ASR circuit•DRN activation decreases and DRN serotonin depletion enhances ASR habituation•Differences in DRN sensory activation and ASR habituation co-segregate The mechanisms of vertebrate behavioral individuality are poorly understood. Pantoja et al. find that differences between individuals in sensory-evoked neuromodulatory input modulate behavior and co-segregate with behavioral differences in a sensory-evoked adaptive behavior. Thus, variation between individuals in neuromodulation contributes to behavioral individuality.