title: Social Status-Dependent Shift in Neural Circuit Activation Affects Decision Making.
abstract: In a social group, animals make behavioral decisions that fit their social ranks. These behavioral choices are dependent on the various social cues experienced during social interactions. In vertebrates, little is known of how social status affects the underlying neural mechanisms regulating decision-making circuits that drive competing behaviors. Here, we demonstrate that social status in zebrafish (Danio rerio) influences behavioral decisions by shifting the balance in neural circuit activation between two competing networks (escape and swim). We show that socially dominant animals enhance activation of the swim circuit. Conversely, social subordinates display a decreased activation of the swim circuit, but an enhanced activation of the escape circuit. In an effort to understand how social status mediates these effects, we constructed a neurocomputational model of the escape and swim circuits. The model replicates our findings and suggests that social status-related shift in circuit dynamics could be mediated by changes in the relative excitability of the escape and swim networks. Together, our results reveal that changes in the excitabilities of the Mauthner command neuron for escape and the inhibitory interneurons that regulate swimming provide a cellular mechanism for the nervous system to adapt to changes in social conditions by permitting the animal to select a socially appropriate behavioral response.SIGNIFICANCE STATEMENTUnderstanding how social factors influence nervous system function is of great importance. Using zebrafish as a model system, we demonstrate how social experience affects decision making to enable animals to produce socially appropriate behavior. Based on experimental evidence and computational modeling, we show that behavioral decisions reflect the interplay between competing neural circuits whose activation thresholds shift in accordance with social status. We demonstrate this through analysis of the behavior and neural circuit responses that drive escape and swim behaviors in fish. We show that socially subordinate animals favor escape over swimming, while socially dominants favor swimming over escape. We propose that these differences are mediated by shifts in relative circuit excitability.
authors.affiliation: Departments of Biology and.
authors.forename: Thomas H
authors.identifier: 0000-0002-8581-3929
authors.initials: TH
authors.lastname: Miller
authors.affiliation: Departments of Biology and.
authors.forename: Katie
authors.initials: K
authors.lastname: Clements
authors.affiliation: Mathematics, East Carolina University, Greenville, North Carolina 27858.
authors.forename: Sungwoo
authors.identifier: 0000-0003-3033-0468
authors.initials: S
authors.lastname: Ahn
authors.affiliation: Department of Mathematics, North Carolina Agricultural and Technical State University, Greensboro, North Carolina 27411, and.
authors.forename: Choongseok
authors.identifier: 0000-0003-4079-8398
authors.initials: C
authors.lastname: Park
authors.affiliation: School of Dentistry, University of California, Los Angeles, California 90096.
authors.forename: Eoon
authors.identifier: 0000-0002-2323-8906
authors.initials: E
authors.lastname: Hye Ji
authors.affiliation: Departments of Biology and issaf14@ecu.edu.
authors.forename: Fadi A
authors.identifier: 0000-0001-5234-5850
authors.initials: FA
authors.lastname: Issa
mesh_terms: D000161:Acoustic Stimulation; D000200:Action Potentials; D000704:Analysis of Variance; D000818:Animals; D001306:Auditory Pathways / Q000502:physiology; D003198:Computer Simulation; D003657:Decision Making / Q000502:physiology*; D004924:Escape Reaction / Q000502:physiology; D007395:Interneurons / Q000502:physiology*; D008297:Male; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D011930:Reaction Time / Q000502:physiology; D013216:Reflex, Startle / Q000502:physiology; D012930:Social Dominance; D013550:Swimming; D015027:Zebrafish
keywords: Mauthner; decision making; dominance; motor control; social regulation; zebrafish