Cortical neurons can be strongly or weakly coupled to the network in which they are embedded, firing in sync with the majority or firing independently. Both these scenarios have potential computational advantages in motor cortex. Commands to the body might be more robustly conveyed by a strongly coupled population, whereas a motor code with greater information capacity could be implemented by neurons that fire more independently. Which of these scenarios prevails? Here we measure neuron-to-body coupling and neuron-to-population coupling for neurons in motor cortex of freely moving rats. We find that neurons with high and low population coupling coexist, and that population coupling was tunable by manipulating inhibitory signaling. Importantly, neurons with different population coupling tend to serve different functional roles. Those with strong population coupling are not involved with body movement. In contrast, neurons with high neuron-to-body coupling are weakly coupled to other neurons in the cortical population.
A key aspect of behavioral inhibition is the ability to wait before acting. Failures in this form of inhibition result in impulsivity and are commonly observed in various neuropsychiatric disorders. Prior evidence has implicated medial frontal cortex, motor cortex, orbitofrontal cortex (OFC), and ventral striatum in various aspects of inhibition. Here, using distributed recordings of brain activity [with local-field potentials (LFPs)] in rodents, we identified oscillatory patterns of activity linked with action and inhibition. Low-frequency (δ) activity within motor and premotor circuits was observed in two distinct networks, the first involved in cued, sensory-based responses and the second more generally in both cued and delayed actions. By contrast, θ activity within prefrontal and premotor regions (medial frontal cortex, OFC, ventral striatum, and premotor cortex) was linked with inhibition. Connectivity at θ frequencies was observed within this network of brain regions. Interestingly, greater connectivity between primary motor cortex (M1) and other motor regions was linked with greater impulsivity, whereas greater connectivity between M1 and inhibitory brain regions (OFC, ventral striatum) was linked with improved inhibition and diminished impulsivity. We observed similar patterns of activity on a parallel task in humans: low-frequency activity in sensorimotor cortex linked with action, θ activity in OFC/ventral prefrontal cortex (PFC) linked with inhibition. Thus, we show that δ and θ oscillations form distinct large-scale networks associated with action and inhibition, respectively.
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