Interoceptive Signals Bias Decision Making in Rhesus Macaques

Abstract

Several influential theories have proposed that interoceptive signals, sent from the body to the brain, contribute to neural processes that coordinate complex behaviors. We altered the physiological state of the body using compounds that have minimal effect on the brain 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 state in the periphery, that was indexed by increased heart rate. Rhesus monkeys were trained on two variants of an approach-avoidance conflict task. The tasks offered a choice 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 was used as a measure of monkeys tolerance for contact with a hot but not painful stimulus or airflow directed at their muzzle. Both drugs reduced tolerance for the aversive stimuli. To determine whether the drug-induced autonomic state 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 in the periphery selectively reduces tolerance for aversive stimuli without altering reward-seeking behaviors. As the drugs used are expected to have little or no direct effect on the brain, the observed biases in decision making are likely induced by interoceptive afferents that signal to the brain the physiological state of the body. Significance statementThe brain adjusts body physiology to the behavioral agenda of the organism through autonomic efferents; concomitantly interoceptive afferents carry signals that inform the brain about the physiological state of the body, closing a homeostatic regulatory loop. Persuasive theories proposed that interoceptive afferents contribute to higher cognitive functions, including emotion. Empirical evidence that these signals are sufficient to bias complex behavior has been limited by the difficulty of isolating interoceptive afferents from the rest of the homeostatic loop. Here we selectively manipulated the autonomic state of the body using drugs with limited penetrance of the brain in macaques performing decision-making tasks. Sympathetic-dominated peripheral states significantly altered decision making, suggesting that changes in interoceptive afferent signals are sufficient to bias behavior.