Neuronal correlates of visual time perception at brief timescales

Abstract

Successful interaction with the world depends on accurate perception of the timing of external events. Neurons at early stages of the primate visual system represent time-varying stimuli with high precision. However, it is unknown whether this temporal fidelity is maintained in the prefrontal cortex, where changes in neuronal activity generally correlate with changes in perception. One reason to suspect that it is not maintained is that humans experience surprisingly large fluctuations in the perception of time. To investigate the neuronal correlates of time perception, we recorded from neurons in the prefrontal cortex and midbrain of monkeys performing a temporal-discrimination task. Visual time intervals were presented at a timescale relevant to natural behavior (<500 ms). At this brief timescale, neuronal adaptationtime-dependent changes in the size of successive responsesoccurs. We found that visual activity fluctuated with timing judgments in the prefrontal cortex but not in comparable midbrain areas. Surprisingly, only response strength, not timing, predicted task performance. Intervals perceived as longer were associated with larger visual responses and shorter intervals with smaller responses, matching the dynamics of adaptation. These results suggest that the magnitude of prefrontal activity may be read out to provide temporal information that contributes to judging the passage of time.vision | frontal eye field | superior colliculus | macaque | latency S ystems neuroscience research has focused on the spatial aspects of vision, including form, orientation, and size (1, 2). However, the role of time in vision is no less important. Research on the temporal aspects of primate vision has largely consisted of studies of the temporal dynamics of neural activity in the early stages of visual processing, where neurons are exquisitely sensitive to changes in spatial and temporal frequency (3, 4). Neuronal correlates of visual timing in higher-order visual areas, and potential associations between that activity and the perception of timing, remain unexplored.A major consideration when studying primate vision is that it is interrupted by saccadic eye movements. Consequently, each "snapshot" of the visual world, during an intersaccadic interval, is less than a half-second long (5). The accurate perception of time intervals at such brief timescales is important in itself (e.g., for estimating the speed of briefly appearing objects) and is elemental for longer timing judgments that span multiple saccades. However, despite a growing interest in time estimation in the visual system (6), few experiments have studied it at subsecond timescales.Our overall goal was to determine the relationship between neuronal activity and the perception of visual timing at subsecond timescales. The simplest possibility is that the latency of sensory responses dictates subsecond temporal perception. However, this straightforward hypothesis is complicated by the fact that visual time perception can vary on the order of tens to hundreds o...

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