Stimulus Context and Reward Contingency Induce Behavioral Adaptation in a Rodent Tactile Detection Task

• Published in: The Journal of neuroscience Vol. 39; no. 6; pp. 1088 - 1099
• Main Authors: Waiblinger, Christian, Wu, Caroline M, Bolus, Michael F, Borden, Peter Y, Stanley, Garrett B
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 06.02.2019
• Subjects: Accumulation; Adaptation; Adaptation, Psychological - physiology; Animal models; Animals; Behavior; Conditioning, Operant - physiology; Contingency; Female; Physical Stimulation; Probabilistic inference; Probabilistic models; Psychomotor Performance - physiology; Psychophysics; Quantitative psychology; Rats; Rats, Sprague-Dawley; Reaction Time; Reinforcement; Reward; Sensory evaluation; Tactile stimuli; Touch - physiology; Vibrissae; Vibrissae - innervation; Vibrissae - physiology; adaptive; behavior; psychophysics; whisker; decision making; rodent
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2032-18.2018

Behavioral adaptation is a prerequisite for survival in a constantly changing sensory environment, but the underlying strategies and relevant variables driving adaptive behavior are not well understood. Many learning models and neural theories consider probabilistic computations as an efficient way to solve a variety of tasks, especially if uncertainty is involved. Although this suggests a possible role for probabilistic inference and expectation in adaptive behaviors, there is little if any evidence of this relationship experimentally. Here, we investigated adaptive behavior in the rat model by using a well controlled behavioral paradigm within a psychophysical framework to predict and quantify changes in performance of animals trained on a simple whisker-based detection task. The sensory environment of the task was changed by transforming the probabilistic distribution of whisker deflection amplitudes systematically while measuring the animal's detection performance and corresponding rate of accumulated reward. We show that the psychometric function deviates significantly and reversibly depending on the probabilistic distribution of stimuli. This change in performance relates to accumulating a constant reward count across trials, yet it is exempt from changes in reward volume. Our simple model of reward accumulation captures the observed change in psychometric sensitivity and predicts a strategy seeking to maintain reward expectation across trials in the face of the changing stimulus distribution. We conclude that rats are able maintain a constant payoff under changing sensory conditions by flexibly adjusting their behavioral strategy. Our findings suggest the existence of an internal probabilistic model that facilitates behavioral adaptation when sensory demands change. The strategy animals use to deal with a complex and ever-changing world is a key to understanding natural behavior. This study provides evidence that rodent behavioral performance is highly flexible in the face of a changing stimulus distribution, consistent with a strategy to maintain a desired accumulation of reward.