Interoceptive Signals Bias Decision Making in Rhesus Macaques

• Published in: bioRxiv
• Main Authors: Cardenas, Michael A, Le, Ryan P, Champ, Tess M, O'Neill, Derek, Fuglevand, Andrew J, Gothard, Katalin M
• Format: Journal Article
• Language: English
• Published: United States Cold Spring Harbor Laboratory 11.07.2024
• Subjects: autonomic; Minor: Neuroscience; decision making; Glycopyrrolate; approach-avoidance conflict; brain-body connection; tachycardia; Atenolol; Isoproterenol; avoidance; approach; Major: Biological Sciences
• ISSN: 2692-8205; 2692-8205
• DOI: 10.1101/2024.07.08.602563

Several 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.