Dataset Information

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.

SUBMITTER: Goc GL

PROVIDER: S-EPMC8456632 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Animals engaged in naturalistic behavior can exhibit a large degree of behavioral variability even under sensory invariant conditions. Such behavioral variability can include not only variations of the same behavior, but also variability across qualitatively different behaviors driven by divergent cognitive states, such as fight-or-flight decisions. However, the neural circuit mechanisms that generate such divergent behaviors across trials are not well understood. To investigate this question, here we studied the visual-evoked responses of larval zebrafish to moving objects of various sizes, which we found exhibited highly variable and divergent responses across repetitions of the same stimulus. Given that the neuronal circuits underlying such behaviors span sensory, motor, and other brain areas, we built a novel Fourier light field microscope which enables high-resolution, whole-brain imaging of larval zebrafish during behavior. This enabled us to screen for neural loci which exhibited activity patterns correlated with behavioral variability. We found that despite the highly variable activity of single neurons, visual stimuli were robustly encoded at the population level, and the visual-encoding dimensions of neural activity did not explain behavioral variability. This robustness despite apparent single neuron variability was due to the multi-dimensional geometry of the neuronal population dynamics: almost all neural dimensions that were variable across individual trials, i.e. the "noise" modes, were orthogonal to those encoding for sensory information. Investigating this neuronal variability further, we identified two sparsely-distributed, brain-wide neuronal populations whose pre-motor activity predicted whether the larva would respond to a stimulus and, if so, which direction it would turn on a single-trial level. These populations predicted single-trial behavior seconds before stimulus onset, indicating they encoded time-varying internal modulating behavior, perhaps organizing behavior over longer timescales or enabling flexible behavior routines dependent on the animal's internal state. Our results provide the first whole-brain confirmation that sensory, motor, and internal variables are encoded in a highly mixed fashion throughout the brain and demonstrate that de-mixing each of these components at the neuronal population level is critical to understanding the mechanisms underlying the brain's remarkable flexibility and robustness.