Learning and Motivation State Fluctuations from Motoric and Neurophysiologic Metrics during a Somatosensory Task in Mice.

Animal learning can be analyzed on two timescales: task acquisition across training sessions and motivation fluctuations within training sessions. How do variations in motor and neurophysiologic activity relate to task performance over these timescales? Here, this question was examined in head-fixed mice performing a whisker-based sensory discrimination task. Male mice were trained for 12-14 daily sessions on a go/no-go task, each lasting ∼1 h to capture spontaneous performance fluctuations over minutes. Simultaneous to task performance, "nonperformance variables" were tracked, including wheel running, pupil size, eyelid aperture, and sensory cortical activity. First, motivation states were defined based on performance tendencies over minutes, leading to three state categories: persistent, disengaged, or attentive. Nonperformance variables were found to predict these states independent of task correctness. Then, when further parsing these states by the go/no-go outcomes of hit, miss, false alarm, or correct rejection, learning-like changes were detected in wheel running, eye movements, and brain activity. Thus, learning over days and motivation fluctuations over minutes form a continuum, as evidenced by changes in motor and physiologic activity variables not directly controlled by task contingencies, even during periods of suboptimal performance in well-trained subjects. These findings improve the understanding of performance variations and implicit learning, in addition to contributing a framework for the analysis of task performance indirectly from motor and neurophysiologic activity.