Stringer, C;
Pachitariu, M;
Steinmetz, N;
Reddy, C;
Carandini, M;
Harris, K;
(2019)
Spontaneous Behaviors Drive Multidimensional, Brain-wide Activity.
Science
, 364
(6437)
, Article eaav7893. 10.1126/science.aav7893.
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Abstract
INTRODUCTION In the absence of sensory inputs, the brain produces structured patterns of activity, which can be as large as or larger than sensory-driven activity. Ongoing activity exists even in primary sensory cortices and has been hypothesized to reflect recapitulation of previous sensory experiences, or expectations of possible sensory events. Alternatively, ongoing activity could be related to behavioral and cognitive states. RATIONALE Much previous work has linked spontaneous neural activity to behavior through one-dimensional measures like running speed and pupil diameter. However, mice perform diverse behaviors consisting of whisking, licking, sniffing, and other facial movements. We hypothesized that there exists a multidimensional representation of behavior in visual cortex and that previously reported “noise” during stimulus presentations may in fact be behaviorally driven. To investigate this, we recorded the activity of ~10,000 neurons in visual cortex of awake mice using two-photon calcium imaging, while simultaneously monitoring the facial movements using an infrared camera. In a second set of experiments, we recorded the activity of thousands of neurons across the brain using eight simultaneous Neuropixels probes, again videographically monitoring facial behavior. RESULTS First, we found that ongoing activity in visual cortex is high dimensional: More than a hundred latent dimensions could be reliably extracted from the population activity. We found that a third of this activity could be predicted by a multidimensional model of the mouse’s behavior, extracted from the face video. This behaviorally related activity was not limited to visual cortex. We observed multidimensional representations of behavior in electrophysiological recordings from frontal, sensorimotor, and retrosplenial cortex; hippocampus; striatum; thalamus; and midbrain. Even though both behavior and neural activity contained fast–time scale fluctuations on the order of 200 ms, they were only related to each other at a time scale of about 1 s. We next investigated how this spontaneous, behavior-related signal interacts with stimulus responses. The representation of sensory stimuli and behavioral variables was mixed in the same neurons: The fractions of each neuron’s variance explained by stimuli and by behavior were only slightly negatively correlated, and neurons with similar stimulus responses did not have more similar behavioral correlates. Nevertheless, at a population level, the neural dimensions encoding motor variables overlapped with those encoding visual stimuli along only one dimension, which coherently increased or decreased the activity of the entire population. Activity in all other behaviorally driven dimensions continued unperturbed regardless of sensory stimulation. CONCLUSION The brainwide representation of behavioral variables suggests that information encoded nearly anywhere in the forebrain is combined with behavioral state variables into a mixed representation. We found that these multidimensional signals are present both during ongoing activity and during passive viewing of a stimulus. This suggests that previously reported noise during stimulus presentations may consist primarily of behavioral-state information. What benefit could this ubiquitous mixing of sensory and motor information provide? The most appropriate behavior for an animal to perform at any moment depends on the combination of available sensory data, ongoing motor actions, and purely internal variables such as motivational drives. Integration of sensory inputs with motor actions must therefore occur somewhere in the nervous system. Our data indicate that it happens as early as primary sensory cortex.
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