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Whole-brain dynamics underlying self-generated behaviour

Periodic Reporting for period 3 - Spontaneous ZeBrain (Whole-brain dynamics underlying self-generated behaviour)

Reporting period: 2020-05-01 to 2021-10-31

Past and current studies that investigated the neuronal basis self-generated behaviours mainly focus on the readiness potential (RP) signal, a build-up ramping activity in the premotor cortex, occurring ~ 2 sec before the movement's onset. However, the neuronal mechanisms underlying the generation of self-generated behaviours (how RPs are generated), the involvement of other regions, and how the brain codes the impending movements (activity predictive of the onset and type of movement), still remain poorly understood.
In this project, we will address these open questions using the zebrafish larva model which enables monitoring whole-brain dynamics in an intact behaving vertebrate. Specifically, we will ask:
1) What is the brain representation and mechanisms underlying self-generated behaviours.
2) A comparison between the neuronal pathways underlying the initiation of self-generated and sensory
induced behaviours.
3) The internal and external modulation of self-generated behaviours.

In other words, we will shed light on how internal decisions are generated in the brain. What are the mechanisms that underlie the emergence of the the intrinsic brain activity predictive of a self-generated behaviour, and which information does this activity carry about the impeding motor behaviour.

This project concerns fundamental science. Therefore, in the short term it will have no practical applications. However, it will provide a lot of novel knowledge to the scientific community and the society in general.
A lot is known about the neural basis of decision making when the brain has to decide over several external sensory stimuli. However, this is not the case on how internal decision are generated.
As a first step, we have developed a custom-made light-sheet microscope that allows recording whole-brain dynamics with near single-neuron resolution while the zebrafish is virtually behaving.
We also developed a pipeline to analyse the calcium imaging data and the kinematics of the motor behaviour..
Our first article was published by the end of 2018, where we studied the spontaneous whole-brain dynamics within the framework of criticality. In this study we found that self-generated motor behaviour deviate the critical state of the brain to a more sub-critical one, momentarily reducing the entire repertoire of potential behaviours, thus allowing the zebrafish larva to engage in coherent motor behaviours (e.g. efficient foraging strategies). This is supported by the observation that consecutive movements are more likely to have a similar laterality if they were chained within less than 10 s than for longer inter-bout intervals.
Along the same lines, sensory interactions with the external environment limited the potential sensory responses to comply with the expectations about the detected stimulus.
This study was published in :Ponce-Alvarez, A., Jouary, A., Privat, M., Deco, G., and Sumbre, G. (2018). Whole-Brain Neuronal Activity Displays Crackling Noise Dynamics. Neuron 100, 1446-1459.e6. doi:10.1016/j.neuron.2018.10.045.

In a second study, we took advantage of the auditory system of the zebrafish larva. In this study, we found a topographic and functional continuum of the sensorimotor representation, suggesting a gradual transformation of sensory information into motor patterns. In addition, we observed an increase in the duration of the auditory-induced calcium transients when a stimulus induced a motor behavior. All together, we suggest that the sensorimotor transformations do not reflect a gating mechanism (e.g. controlling the passage of neuronal activity from the sensory to the motor circuits by an independent modulatory circuit) but rather the capacity of the circuit to integrate the auditory-induced neuronal response. This hypothesis is also supported by the long and variable latency of the induced tail movements. The increase in the duration of the calcium transients could be driven through recurrent connectivity to sufficiently amplify neural activity and reach the threshold required to activate the motor circuits. We suggest that thisn mechanism may help integrate auditory information to obtain reliable information about the detected stimulus to generate a relevant behavioral response.
This study was published in:
Privat, M., Romano, S. A., Pietri, T., Jouary, A., Boulanger-Weill, J., Elbaz, N., et al. (2019). Sensorimotor Transformations in the Zebrafish Auditory System. Curr. Biol., 1–14. doi:10.1016/j.cub.2019.10.020.
We have succeeded in monitoring whole-brain dynamics with single-neuron resolution in an intact behaving vertebrate. We have improved our SPIM and we can now record the activity of 70-80% of the larva's ~100,000 neurons before the execution of self-generated behaviours.
Using immunochemistry, we are now capable of also identifying the cell type of each recorded neuron.
For data analysis we developed several software, using approaches of data mining, graph theory and topology.
spontaneous activity predictive of the onset of a self-generated movement
the developed light imaging setup