Slow drift of neural activity as a signature of impulsivity in macaque visual and prefrontal cortex

Abstract

An animal's decision depends not only on incoming sensory evidence but also on its fluctuating internal state. This internal state is a product of cognitive factors, such as fatigue, motivation, and arousal, but it is unclear how these factors influence the neural processes that encode the sensory stimulus and form a decision. We discovered that, over the timescale of tens of minutes during a perceptual decision-making task, animals slowly shifted their likelihood of reporting stimulus changes. They did this unprompted by task conditions. We recorded neural population activity from visual area V4 as well as prefrontal cortex, and found that the activity of both areas slowly drifted together with the behavioral fluctuations. We reasoned that such slow fluctuations in behavior could either be due to slow changes in how the sensory stimulus is processed or due to a process that acts independently of sensory processing. By analyzing the recorded activity in conjunction with models of perceptual decision-making, we found evidence for the slow drift in neural activity acting as an impulsivity signal, overriding sensory evidence to dictate the final decision. Overall, this work uncovers an internal state embedded in the population activity across multiple brain areas, hidden from typical trial-averaged analyses and revealed only when considering the passage of time within each experimental session. Knowledge of this cognitive factor was critical in elucidating how sensory signals and the internal state together contribute to the decision-making process.

The eyes reflect an internal cognitive state hidden in the population activity of cortical neurons

“…Previously we reported a slow fluctuation in neural activity in V4 and PFC that we termed 'slow drift' [58]. We found that this neural signature was related to the subject's tendency to make impulsive decisions in a change detection task, ignoring sensory evidence (false alarms).…”

“…We recorded from neurons in 1) V4 while the subjects performed an orientation-change detection task ( Figure 1A); and 2) PFC while they performed a memory-guided saccade task ( Figure 1B). Data from each task has been published previously [58,60]. However, the main goal of this study was to determine whether the neural population activity was related to eye metrics in a predictable manner across tasks.…”

“…The width of the window, and the step size, were chosen to isolate slow changes over time based on previous research. They were the same as those used by Cowley et al [58], which meant direct comparisons could be made across studies. An example session from the same subject on the change detection task and the memory-guided saccade task is shown in Figure 2C and Figure 2D, respectively.…”

“…from a single trial. To isolate slow changes, the data was binned using a 30-minute sliding window stepped every 6 minutes (solid line) [58]. (B) Same as (A) but for the memory-guided saccade task.…”

“…However, if changes in these eye metrics are driven by a shift in an underlying internal state, then one might expect them all to be related to a common underlying neural activity pattern. Recent work in our laboratory used dimensionality reduction to identify a dominant mode of neural activity called slow drift that was related to behavior in a change detection task and present in both visual and prefrontal cortex in the macaque [58]. If such a prevalent change in brain-wide neural activity was truly reflective of a changing internal state, then it might also be reflective of wideranging changes in behavior.…”