Thermal modulation of Zebrafish exploratory statistics reveals constraints on individual behavioral variability

Background: Variability is a hallmark of animal behavior. It contributes
to survival by endowing individuals and populations with the capacity to
adapt to ever-changing environmental conditions. Intra-individual
variability is thought to reflect both endogenous and exogenous
modulations of the neural dynamics of the central nervous system. However,
how variability is internally regulated and modulated by external cues
remains elusive.  Here we address this question by analyzing the
statistics of spontaneous exploration of freely swimming zebrafish larvae,
and by probing how these locomotor patterns are impacted when changing the
water temperatures within an ethologically relevant range. Results: We
show that, for this simple animal model, five short-term kinematic
parameters - interbout interval, turn amplitude, travelled distance, turn
probability and orientational flipping rate - together control the
long-term exploratory dynamics. We establish that the bath temperature
consistently impacts the means of these parameters, but leave their
pairwise covariance unchanged. These results indicate that the temperature
merely controls the sampling statistics within a well-defined kinematic
space delineated by this robust statistical structure. At a given
temperature, individual animals explore the behavioral space over a
timescale of tens of minutes, suggestive of a slow internal state
modulation that could be externally biased through the bath temperature.
By combining these various observations into a minimal stochastic model of
navigation, we show that this thermal modulation of locomotor kinematics
results in a thermophobic behavior, complementing direct gradient-sensing
mechanisms. Conclusions: This study establishes the existence of a
well-defined locomotor space accessible to zebrafish larvae during
spontaneous exploration, and quantifies self-generated modulation of
locomotor patterns. Intra-individual variability reflects a slow
diffusive-like probing of this space by the animal. The bath temperature
in turn restricts the sampling statistics to sub-regions, endowing the
animal with basic thermophobicity. This study suggests that in Zebrafish,
as well as in other ectothermic animals, ambient temperature could be used
to efficiently manipulate internal states in a simple and ethological way.