Global, Low-Amplitude Cortical State Predicts Response Outcomes in a Selective Detection Task in Mice

Abstract

Spontaneous neuronal activity strongly impacts stimulus encoding and behavioral responses. We sought to determine the effects of neocortical prestimulus activity on stimulus detection. We trained mice in a selective whisker detection task, in which they learned to respond (lick) to target stimuli in one whisker field and ignore distractor stimuli in the contralateral whisker field. During expert task performance, we used widefield Ca2+ imaging to assess prestimulus and post-stimulus neuronal activity broadly across frontal and parietal cortices. We found that lower prestimulus activity correlated with enhanced stimulus detection: lower prestimulus activity predicted response versus no response outcomes and faster reaction times. The activity predictive of trial outcome was distributed through dorsal neocortex, rather than being restricted to whisker or licking regions. Using principal component analysis, we demonstrate that response trials are associated with a distinct and less variable prestimulus neuronal subspace. For single units, prestimulus choice probability was weak yet distributed broadly, with lower than chance choice probability correlating with stronger sensory and motor encoding. These findings support low amplitude and low variability as an optimal prestimulus cortical state for stimulus detection that presents globally and predicts response outcomes for both target and distractor stimuli.

Dorsolateral striatum, not motor cortex, is a bottleneck for responding to task-relevant stimuli in a learned whisker detection task in mice

“…This framework would have predicted positive prestimulus choice probability for target-aligned DLS. In contrast, we find that bilateral DLS, like the rest of dorsal neocortex (Marrero et al, 2021), displays negative prestimulus choice probability in response to target stimuli (Figure 4A, F and Supplemental Figure 1F). This difference may be due to sensory modality or task design.…”

“…We recently reported lower than chance (negative) choice probability before stimulus onset throughout neocortex, indicating that lower prestimulus activity is more likely to result in a response (versus no response) outcome (Marrero et al, 2021). Interestingly, here we observe below chance pre-stimulus choice probability in target-aligned and distractor-aligned DLS as well (Figure 4A, F, H).…”

“…We trained mice in a head-fixed, whisker-based selective detection task (Aruljothi et al, 2020; Marrero et al, 2021; Zareian et al, 2021). In this task, mice learned to respond (lick) to small, transient whisker deflections within one whisker field (target) and to ignore identical whisker deflections in the opposite whisker field (distractor) (Figure 1 A and F).…”

“…We trained mice in a selective detection task, which we have characterized in previous studies (Aruljothi et al, 2020; Marrero et al, 2021; Zareian et al, 2021). The mice were head-fixed in a custom-made setup.…”

Frontal Cortex Gates Distractor Stimulus Encoding in Sensory Cortex

“…Neuronal activity of dorsal cortex was imaged in GCaMP6s expressing mice during expert performance in the selective detection task. The imaging datasets analyzed here were previously published (Aruljothi et al, 2020;Marrero et al, 2022). The dataset consists of n=40 behavioralimaging sessions from n=5 mice.…”