Heading and Then Saccades Predict Visual Discrimination Decisions in Freely Moving Ferrets

Decision-making is a continuous process that manifests as evolving sequences of motor movements while animals navigate the sensory environment. Studying decision-making in a naturalistic setting has been challenging as restrictions are typically imposed on subjects' motor actions in the laboratory. We utilized a novel paradigm in which animals move freely throughout the decision-making process to examine the sequence and timing of motor actions predictive of decisions. We trained freely moving ferrets (two males, three females), highly visual carnivores, to perform visual discrimination tasks and measured their head position and eye movements to assess the temporal dynamics of heading and saccades during visually guided decisions. We discovered that heading revealed ferrets' "turning time" per trial, signaling their choices, and heading on its own best predicted ferrets' decisions. Ferrets made decisions quickly and decisively, although total trial durations varied across animals. Importantly, initial heading, at the beginning of the decision-making process, revealed ferrets' decision biases and task strategies. Ferrets made choice-directed saccades on most trials. Horizontal eye movements and saccades were also predictive of decisions, but saccades followed choice-indicative head turns. These results show that ferrets make quick decisions with minimal visual scanning and then orient first with their heads and then with saccades toward targets displaced by >10°. Furthermore, our findings indicate that heading is the most robust predictor of visually guided decision-making, followed by saccades. Together, these motor actions provide reliable, noninvasive readouts of the temporal dynamics of natural visual decision-making in freely moving subjects.