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

Abstract

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.

Emergence of time persistence in a data-driven neural network model

“…We thus sought to examine whether the thermal dependence of the ARTR endogenous dynamics could manifest itself in the animal navigational statistics. In order to do so, we used the results of a recent study ( Le Goc et al, 2021 ), in which 5 to 7 days old zebrafish larvae were video-monitored as they swam freely at constant and uniform temperature in the same thermal range (Figure 1E). We quantified the time scale of the turn direction persistence by assigning a discrete value to each turn bout: −1 for a right turn, +1 for a left turn (forward scouts were ignored).…”

“…Recent studies have shown that spontaneous behavior in zebrafish larvae is not time-invariant but exhibits transitions between different regimes, lasting over minutes and associated with specific brain-states. These transitions can have no apparent cause ( Le Goc et al, 2021 ) or be induced by external (e.g. stimuli( Andalman et al, 2019 )) or internal cues (e.g.…”

Optokinetic set-point adaptation functions as an internal dynamic calibration mechanism for oculomotor disequilibrium

“…The exploratory behavior of zebrafish reveals overall symmetric distribution between the left and right turning angles ( Dunn et al., 2016 ; Goc et al., 2021 ). Since the general visual experience in real life should be directionally symmetric, we asked ourselves what the physiological necessity of the underlying set-point adaptation is.…”

Ectodermal origins of the skin-brain axis: a novel model for the developing brain, inflammation, and neurodevelopmental conditions

“…In the same period, our cognitive capacity increased emphatically, spurring interest as to whether thermoregulation may influence neural development. Preliminary evidence for this hypothesis stems from recent zebrafish models, where the ambient water temperature was observed to drive persistent changes in exploratory behaviour [ 57 ]. These findings indicate that thermoregulatory mechanisms may drive intra-individual variability in vertebrate kinematics, likely by influencing neural circuits that regulate locomotor control [ 57 ].…”

“…Preliminary evidence for this hypothesis stems from recent zebrafish models, where the ambient water temperature was observed to drive persistent changes in exploratory behaviour [ 57 ]. These findings indicate that thermoregulatory mechanisms may drive intra-individual variability in vertebrate kinematics, likely by influencing neural circuits that regulate locomotor control [ 57 ]. In humans, anecdotal evidence supporting a link between thermoregulation and neurodevelopment can be derived from parental reports of improved social interaction and language ability during febrile states in autistic children [ 58 ].…”