Serotonin neurons modulate learning rate through uncertainty

Grossman, Cooper D.; Bari, Bilal A.; Cohen, Jeremiah Y.

doi:10.1016/j.cub.2021.12.006

Cited by 100 publications

(123 citation statements)

References 120 publications

(188 reference statements)

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“…However, many classic rodent cognitive tasks are species-specific: they were not designed to assess the same cognitive processes across species, and this limits their translational ability. Currently, there is an emerging exciting trend among rodent researchers with adopting tasks with translational potentials in rodents, such as reversal learning and various versions of bandit task ( Izquierdo et al, 2019 ; Groman et al, 2016 ; Bari et al, 2019 ; Grossman et al, 2021 ), where we can assess the same cognitive processes across species and across animal models of diseases. Here, we establish that explore-exploit decisions are shared cognitive processes across species, making this restless bandit task an ideal tool for translational research.…”

Section: Discussionmentioning

confidence: 99%

Sex differences in learning from exploration

Chen

Knep

Han

et al. 2021

eLife

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Sex-based modulation of cognitive processes could set the stage for individual differences in vulnerability to neuropsychiatric disorders. While value-based decision making processes in particular have been proposed to be influenced by sex differences, the overall correct performance in decision making tasks often show variable or minimal differences across sexes. Computational tools allow us to uncover latent variables that define different decision making approaches, even in animals with similar correct performance. Here, we quantify sex differences in mice in the latent variables underlying behavior in a classic value-based decision making task: a restless 2-armed bandit. While male and female mice had similar accuracy, they achieved this performance via different patterns of exploration. Male mice tended to make more exploratory choices overall, largely because they appeared to get 'stuck' in exploration once they had started. Female mice tended to explore less but learned more quickly during exploration. Together, these results suggest that sex exerts stronger influences on decision making during periods of learning and exploration than during stable choices. Exploration during decision making is altered in people diagnosed with addictions, depression, and neurodevelopmental disabilities, pinpointing the neural mechanisms of exploration as a highly translational avenue for conferring sex-modulated vulnerability to neuropsychiatric diagnoses.

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Section: Discussionmentioning

confidence: 99%

Sex differences in learning from exploration

Chen

Knep

Han

et al. 2021

eLife

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“…Serotonin is a neuromodulatory neurotransmitter produced in the brainstem raphe nuclei and released throughout the nervous system. The serotonergic system is involved in a wide range of behaviors, including emotional behaviors such as the response to rewards (Liu et al, 2014;Hu, 2016;Xu et al, 2017;Wei et al, 2018), punishments (Cohen et al, 2015), anxiety-and depression-related behaviors (Lowry et al, 2005;Hale et al, 2012;Teissier et al, 2015;Dolzani et al, 2016;Urban et al, 2016;Natarajan et al, 2017;Nishitani et al, 2018), social interaction (Bala ´zsfi et al, 2018;Walsh et al, 2018), aggression (Nautiyal et al, 2015;Coccaro et al, 2015), and learning rate (Grossman et al, 2022;Iigaya et al, 2018). The raphe nuclei likewise send projections to nearly every area of the brain.…”

Section: Introductionmentioning

confidence: 99%

Single-cell activity and network properties of dorsal raphe nucleus serotonin neurons during emotionally salient behaviors

Paquelet

Carrion

Lacefield

et al. 2022

Neuron

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“…However, the detailed mechanisms by which central ACh affects pupil size remain unknown. Moreover, recent studies have reported that the activity of the dorsal raphe nucleus (DRN) serotonin neurons in mice also tracks environmental uncertainty (101) and that photoactivation of DRN 5-HT neurons also elicits pupil dilation (102). However, the bidirectional connection between DRN and LC (83) further complicates this relationship.…”

Section: Limitations and Open Questionsmentioning

confidence: 99%

Pupil diameter tracked during motor adaptation in humans

Yokoi

Weiler

2021

Preprint

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Research in reward-based decision-making showed that humans and animals dynamically modulate learning rate according to their belief about environmental change (volatility) and surprise about observation. Recent evidence also suggests that neuromodulator noradrenaline (NA) signals volatility and surprise. Despite the rich anatomical evidence suggesting the potential influence of NA on the motor system, it is still elusive how NA and volatility/surprise affect human motor learning. To address this issue, we ran a series of experiments in which we simultaneously tracked the pupil diameter, a non-invasive proxy for the central NA/arousal activity, during a short-term force-field reach adaptation paradigm. A sudden increase in error due to the force-field resulted in increased pupil dilation during movement followed by an elevated baseline diameter in the following trials. These online and offline pupil responses showed a consistent pattern with surprise and volatility simulated by a recent computational model which dynamically adjusts learning rate according to volatility estimated from experienced error (surprise). However, unlike the model's prediction, when participants experienced frequent reversals in force-field, the size of pupil responses rapidly diminished regardless of large errors induced by reversals. We further confirmed that the causal manipulation of participants' arousal by task-irrelevant auditory stimuli modulated the single-trial motor learning rate. Collectively, these results provide a compelling evidence that NA/arousal system acts as a common modulator of learning rate in both cognitive and motor domains. Rapid reduction in pupil responses at reversals suggests that error sensitivity for computing current environmental uncertainty and surprise is also highly dynamic.

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Serotonin neurons modulate learning rate through uncertainty

Cited by 100 publications

References 120 publications

Sex differences in learning from exploration

Sex differences in learning from exploration

Single-cell activity and network properties of dorsal raphe nucleus serotonin neurons during emotionally salient behaviors

Pupil diameter tracked during motor adaptation in humans

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