Interoceptive Signals Bias Decision Making in Rhesus Macaques

Abstract

AbstractSeveral influential theories have proposed that interoceptive signals, sent from the body to the brain, contribute to neural processes that coordinate complex behaviors. Using pharmacological agents that do not cross the blood-brain barrier, we altered interoceptive states and evaluated their effect on decision-making in rhesus monkeys. We used glycopyrrolate, a non-specific muscarinic (parasympathetic) antagonist, and isoproterenol, a beta-1/2 (sympathetic) agonist, to create a sympathetic-dominated physiological state indexed by increased heart rate. Rhesus monkeys were trained on two variants of an approach-avoidance conflict task, where they chose between enduring mildly aversive stimuli in exchange for a steady flow of rewards, or cancelling the aversive stimuli, forgoing the rewards. The delay to interrupt the aversive stimuli and the reward were used as a measure of the cost-benefit estimation that drove the monkeys’ decisions. Both drugs altered approach-avoidance decisions, substantially reducing the delay to interrupt the aversive stimuli. To determine whether this autonomic state lowered tolerance to aversive stimuli or reduced the subjective value of the reward, we tested the effects of glycopyrrolate on a food preference task. Food preference was unaltered, suggesting that the sympathetic dominated state selectively reduces tolerance for aversive stimuli without altering reward-seeking behaviors. As these drugs have no direct effect on brain physiology, interoceptive afferents are the most likely mechanism by which decision making was biased toward avoidance.Significance statementInfluential theories have proposed that the organs of the body send information to the brain and these signals contribute to higher cognitive functions including emotion. Concomitantly, the brain adjusts body physiology to the behavioral agenda of the organism. Empirical support for these ideas, however, has been limited because of the difficulty of dissociating the contributions of brain circuits and body physiology to cognitive processing. Here we selectively manipulated the autonomic state of the body using drugs that do not cross the blood-brain barrier while macaques performed complex decision-making tasks. Drugs that induced sustained peripheral sympathetic activity significantly altered decision making. These findings suggest that ascending, interoceptive signals play a critical role in shaping behavior.