Sympathetic and parasympathetic involvement in time constrained sequential foraging

Abstract

Appraising sequential offers relative to an unknown future opportunity and a time cost requires an optimization policy that draws on a learned estimate of an environment's richness. Converging evidence points to a learning asymmetry, whereby estimates of this richness update with a bias toward integrating positive information. We replicate this bias in a sequential foraging (prey selection) task and probe associated activation within two branches of the autonomic system, sympathetic and parasympathetic branches, using trial-by-trial measures of simultaneously recorded cardiac autonomic physiology. In general, lower value offers were accepted during periods of autonomic drive, both in the sympathetic (shorter pre-ejection period PEP) and parasympathetic (higher HF HRV) branches. In addition, we reveal a unique adaptive role for the sympathetic branch in learning. It was specifically associated with adaptation to a deteriorating environment: it correlated with both the rate of negative information integration in belief estimates and downward changes in moment-to-moment environmental richness, and was predictive of optimal performance on the task. The findings are consistent with a parallel processing framework whereby autonomic function serves both learning and executive demands of prey selection. Significance statementThe value of choices (accepting a job) depends on context (richness of the current job market).Learning contexts, therefore, is crucial for optimal decision-making. Humans demonstrate a bias when learning contexts; we learn faster about improvements vs deteriorations. New techniques allow us to cleanly measure fast acting stress responses that might fluctuate with trial-by-trial learning. Using these new methods, we observe here that increased stress -specifically sympathetic (heart contractility) -might help overcome the learning bias (making us faster at learning contextual deterioration) and thereafter guide us toward better context appropriate decisions. For the first time we show that specific building blocks of good decision-making might benefit from short bursts of specific inputs of the stress system.

Cardiac-sympathetic contractility and neural alpha-band power: cross-modal collaboration during approach-avoidance conflict

“…Under this assumption, it would be physiologically efficient to therefore prioritize reward information, and reserve effortful scrutiny and juxtaposition involving multiple streams of information for moments of conflict. Reward-sensitivity also generalizes to dynamic learning tasks, where recent studies report that people learn faster from positive-vs-negative prediction errors 5,[46][47] . Consistent with our present findings, this learning asymmetry attenuates (i.e., learning from negative outcomes occurs more rapidly) when sympathetic activity is elevated 5,48 , to the extent that sympathetic reactivity even predicts individual participants who adjust their behavior more optimally to declining changes in their environment 5 .…”

“…Reward-sensitivity also generalizes to dynamic learning tasks, where recent studies report that people learn faster from positive-vs-negative prediction errors 5,[46][47] . Consistent with our present findings, this learning asymmetry attenuates (i.e., learning from negative outcomes occurs more rapidly) when sympathetic activity is elevated 5,48 , to the extent that sympathetic reactivity even predicts individual participants who adjust their behavior more optimally to declining changes in their environment 5 . Whether cardiacsympathetics serve common mechanisms to resolve uncertainty and address biases across decisions and learning is an exciting avenue of future research.…”

“…Meanwhile, reactivity in peripheral organ systems, such as the cardiac-sympathetic branch, is well documented in tasks requiring momentary goal-directed changes in mental and physical exertion, showing appropriate reactivity (just enough, just in time) to the task at hand [1][2][3] . More recent evidence extends cardiac-sympathetic reactivity to complex cognitive challenges such as value-based decision making 4,5 . However it is not yet fully known whether cardiac-sympathetic reactivity is an epiphenomenal companion or whether it is instead fundamentally intertwined with complex cognitive processes.…”

“…Second, the paradigm can identify prepotent sensitivity toward a particular value dimension, such as the reward sensitivity commonly reported in healthy controls 4,[9][10][11] (Figure 1C). Third, conflict arising from integrated reward and cost recruits a broad array of frontal cortical brain networks 4,8,9,[12][13][14][15][16] , in addition to increased cardiac-sympathetic responses 4,5 , suggesting the paradigm drives qualitative shifts both in behavior and across a complex physiological cascade, allowing us to test cross-modal relations. To decompose behavior even further, and extract fine-grained assays of behavioral perturbations to correlate with physiology signals, we fitted the drift-diffusion model [17][18][19][20][21][22][23][24][25] (DDM) to choice and RT data (Figure 1D).…”

An Accelerometer Based Heart Monitor to Measure Changes of the Autonomic Nervous System

“…PEP in particular has been shown to be a reliable indicator of the sympathetic nervous system (SNS), resulting in an inverse relationship where a decrease in PEP represents an increase in sympathetic activity. PEP is sensitive to the predictive effects of task manipulations (Kelsey et al, 2000(Kelsey et al, , 2004, decision making (Dundon et al, 2020(Dundon et al, , 2021 and Running head: A WEARABLE HEART CONTRACTILITY MONITOR 4 individual differences in a variety of tasks (Kelsey, 1991;Kelsey et al, 2001). LVET is defined by the time interval between the opening and closing of the aortic valve, representing the interval during which the left ventricle ejects blood into the aorta (Figure 1).…”