A low-dimensional signature of global brain state in the superior colliculus of the macaque

Recent work has shown that global signals related to arousal are embedded in the population activity of cortical neurons. In mice, slow fluctuations in neural activity are correlated with whisking and locomotion, while in monkeys a similar pattern has been identified (termed “slow drift”) that is: 1) present in visual/prefrontal cortices; 2) correlated with pupil size; and 3) associated with performance on cognitive tasks. These results demonstrate that changes in brain state are represented in the coordinated activity of cortical neurons. However, it is unknown if these fluctuations are also present in subcortical regions that have been implicated in oculomotor control (e.g., the superior colliculus or SC). One might expect an area close to the motor output to be isolated from such fluctuations, as they could lead to unwanted eye movements. Alternatively, they could still be present in the SC but occupy an orthogonal subspace, which is not readout by downstream regions innervating the oculomotor muscles. To investigate if slow drift is present in the SC, we simultaneously recorded from neuronal populations in the superior colliculus (SC) and prefrontal cortex (PFC) of two monkeys while they performed a memory-guided saccade task. Results showed that the activity of individual SC neurons drifted slowly over time, and when principal component analysis (PCA) was applied to the data it revealed a neural activity pattern that was akin to the slow drift previously reported in cortical neurons. Importantly, slow drift in SC was significantly correlated with slow drift in PFC and the timescale of slow drift in the SC was highly similar to that observed in the PFC. These results indicate the brain-wide nature of slow fluctuations in arousal and pose important questions about how perception and movement can be isolated from slow drifts in neural activity (potentially through isolated subspaces).