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Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment.

ABSTRACT: Decision-making is a continuous and dynamic process with prior experience reflected in and used by the brain to guide adaptive behavior. However, most neurobiological studies constrain behavior and/or analyses to task-related variables, not accounting for the continuous internal and temporal space in which they occur. We show mice rely on information learned through recent and longer-term experience beyond just prior actions and reward - including checking behavior and the passage of time - to guide self-initiated, self-paced, and self-generated actions. These experiences are represented in secondary motor cortex (M2) activity and its projections into dorsal medial striatum (DMS). M2 integrates this information to bias strategy-level decision-making, and DMS projections reflect specific aspects of this recent experience to guide actions. This suggests diverse aspects of experience drive decision-making and its neural representation, and shows premotor corticostriatal circuits are crucial for using selective aspects of experiential information to guide adaptive behavior.

SUBMITTER: Schreiner DC

PROVIDER: S-EPMC9018678 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment.

Schreiner Drew C DC Cazares Christian C Renteria Rafael R Gremel Christina M CM

Nature communications 20220419 1

Decision-making is a continuous and dynamic process with prior experience reflected in and used by the brain to guide adaptive behavior. However, most neurobiological studies constrain behavior and/or analyses to task-related variables, not accounting for the continuous internal and temporal space in which they occur. We show mice rely on information learned through recent and longer-term experience beyond just prior actions and reward - including checking behavior and the passage of time - to g ...[more]

PMID: 35440120

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Project description:In a social group, animals make behavioral decisions that fit their social ranks. These behavioral choices are dependent on the various social cues experienced during social interactions. In vertebrates, little is known of how social status affects the underlying neural mechanisms regulating decision-making circuits that drive competing behaviors. Here, we demonstrate that social status in zebrafish (Danio rerio) influences behavioral decisions by shifting the balance in neural circuit activation between two competing networks (escape and swim). We show that socially dominant animals enhance activation of the swim circuit. Conversely, social subordinates display a decreased activation of the swim circuit, but an enhanced activation of the escape circuit. In an effort to understand how social status mediates these effects, we constructed a neurocomputational model of the escape and swim circuits. The model replicates our findings and suggests that social status-related shift in circuit dynamics could be mediated by changes in the relative excitability of the escape and swim networks. Together, our results reveal that changes in the excitabilities of the Mauthner command neuron for escape and the inhibitory interneurons that regulate swimming provide a cellular mechanism for the nervous system to adapt to changes in social conditions by permitting the animal to select a socially appropriate behavioral response.SIGNIFICANCE STATEMENT Understanding how social factors influence nervous system function is of great importance. Using zebrafish as a model system, we demonstrate how social experience affects decision making to enable animals to produce socially appropriate behavior. Based on experimental evidence and computational modeling, we show that behavioral decisions reflect the interplay between competing neural circuits whose activation thresholds shift in accordance with social status. We demonstrate this through analysis of the behavior and neural circuit responses that drive escape and swim behaviors in fish. We show that socially subordinate animals favor escape over swimming, while socially dominants favor swimming over escape. We propose that these differences are mediated by shifts in relative circuit excitability.

Project description:Actions shape what we see and memorize. A previous study suggested the interaction between motor and memory systems by showing that memory encoding for task-irrelevant items was enhanced when presented with motor-response cues. However, in the studies on the attentional boost effect, it has been revealed that detection of the target stimulus can lead to memory enhancement without requiring overt action. Thus, the direct link between the action and memory remains unclear. To exclude the effect of the target detection process as a potential confounder, this study assessed the benefit of action for memory by separating items from the response cue in time. In our pre-registered online experiment (N = 142), participants responded to visual Go cues by pressing a key (i.e., motor task) or counting (i.e., motor-neutral cognitive task) while ignoring No-go cues. In each trial, two task-irrelevant images were sequentially presented after the cue disappearance. After encoding the Go/No-go tasks, participants performed a surprise recognition memory test for those images. Importantly, we quantified the impact of overt execution of the action by comparing memories with and without motor response and the impact of covert motor processes (e.g., preparation and planning of action) by comparing memory between the motor and cognitive tasks. The results showed no memory differences between Go and No-go trials in the motor task. This means that the execution itself was not critical for memory enhancement. However, the memory performance in the motor No-go trials was higher than that in the cognitive No-go trials, only for the items presented away from the cues in time. Therefore, engaging the motor task itself could increase incidental memory for the task-irrelevant items compared to a passive viewing situation. We added empirical evidence on the online interaction between action and memory encoding. These memory advantages could be especially brought in action preparation and planning. We believe this fact may expand our present understanding of everyday memory, such as active learning.

Dataset Information

Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment.

Publications

Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment.

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