Cerebellar Neurodynamics Predict Decision Timing and Outcome on the Single-Trial Level

Abstract

Goal-directed behavior requires the interaction of multiple brain regions. How these regions and their interactions with brain-wide activity drive action selection is less understood. We have investigated this question by combining whole-brain volumetric calcium imaging using light-field microscopy and an operant-conditioning task in larval zebrafish. We find global, recurring dynamics of brain states to exhibit pre-motor bifurcations towards mutually exclusive decision outcomes. These dynamics arise from a distributed network displaying trial-by-trial functional connectivity changes, especially between cerebellum and habenula, which correlate with decision outcome. Within this network the cerebellum shows particularly strong and predictive pre-motor activity (>10 s before movement initiation), mainly within the granule cells. Turn directions are determined by the difference neuroactivity between the ipsilateral and contralateral hemispheres, while the rate of bi-hemispheric population ramping quantitatively predicts decision time on the trial-by-trial level. Our results highlight a cognitive role of the cerebellum and its importance in motor planning.

Ramp-to-Threshold Dynamics in a Hindbrain Population Controls the Timing of Spontaneous Saccades

“…Furthermore, such studies have shown trial-to-trial variation in the timing of the movement is associated with variation in the ramp rate, with a slower rise coupled to longer rise time, suggesting that action is initiated when neural activity ramps to a cell-specific threshold (Maimon & Assad, 2006;Murakami, Vicente, Costa, & Mainen, 2014). More generally, such ramp-to-threshold dynamics have also been found ahead of goal-directed movements (Lin et al, 2020;Schultz & Romo, 1992b) and in decision-making tasks (Bahl & Engert, 2020;Cain, Barreiro, Shadlen, & Shea-Brown, 2013;Dragomir, Štih, & Portugues, 2020;Gold & Shadlen, 2007;Lin et al, 2020;Scott et al, 2017) where the animal is responding expressly to some externally provided stimulus, leading to the proposal that there may be common principles underlying the generation of ramp-to-threshold activity associated with motor planning for both spontaneous and externally-driven actions (Murakami & Mainen, 2015;Schurger, Sitt, & Dehaene, 2012). However, there are many basic questions unanswered about this ramp-to-threshold dynamic, especially in the spontaneous setting, not only regarding how it is generated, but whether it is preparatory, possibly facilitatory (but not essential), or perhaps suppressive (Ames & Churchland, 2019;Lara, Elsayed, Zimnik, Cunningham, & Churchland, 2018;Wise, Weinrich, & Mauritz, 1986;Wong, Haith, & Krakauer, 2015).…”

Healthy Aging Alters the Functional Connectivity of Creative Cognition in the Default Mode Network and Cerebellar Network

“…In another fMRI study, Stoodley et al ( 2012 ) demonstrated that neural activation patterns within and between cerebro-cerebellar circuits supported cognitive tasks in various domains, including sensorimotor activity, working memory, execution control, language, visuospatial, and affective processing. These findings suggest that cerebro-cerebellar interactions are critical to the coordination of sensorimotor information, control of internally focused attention, retrieval of goal-directed memories, and production of unusual thoughts (Ramnani, 2006 ; Honda et al, 2018 ; Lin et al, 2020 ).…”

“…The CAQ was proposed to assess achievement across 10 domains of creativity using strong psychometric parameters, and is associated with individual differences in the neuroanatomical changes of younger adults (Jung et al, 2010 ). Based on previous neuroimaging studies in which the modulation of the prefrontal cortex and suppression of the DMN decreased with age (i.e., DECHA) (Turner and Spreng, 2015 ; Spreng and Turner, 2019 ), and given the critical supportive role of the cerebro-cerebellar network in higher-level cognition (Ramnani, 2006 ; Honda et al, 2018 ; Lin et al, 2020 ), we hypothesized that healthy older adults would exhibit altered functional connectivity in areas of the DMN, ECN, and CN associated with creative cognition. Furthermore, we hypothesized that individual differences in creative performance would modulate the effectiveness of interactions within and between creativity-associated cerebro-cerebellar networks.…”

Latent dynamical variables produce signatures of spatiotemporal criticality in large biological systems

“…A key problem in modern biological physics is extracting useful knowledge from massive data sets enabled by high-throughput experimentation. For example, now one can record simultaneous states of thousands of neurons [1][2][3][4][5] or gene expressions [6][7][8], or the abundances of species in microbiomes [9][10][11]. Inferring and interpreting the joint probability distributions of so many variables is infeasible.…”