Selective coupling and decoupling coordinate distributed brain networks for precise action.
Stefan M Lemke, Simone Appaqaq, Jian-Zhong Guo, Adam W Hantman
Abstract
Open AccessThe mammalian brain is fundamentally interconnected. Across species, a single neuron typically forms thousands of synapses spanning local and long-range connections. This architecture suggests that brain function is distributed, but it remains poorly understood how relevant networks are selectively engaged to produce appropriate behaviors. To address this, we recorded >40,000 neurons, simultaneously monitoring five cerebellar and cerebral brain areas as mice performed complex motor actions, capturing interactions of >5,000,000 cross-area neuron pairs. This revealed that complex pre-movement cross-area interactions coordinate distributed networks to produce precise and consistent actions. Prior to action production, action-informative neural populations across the brain become coupled, while non-informative populations decouple. This coupling and decoupling was mirrored by two distinct local field potential oscillations linking neuron-level to population-level dynamics. External modulation of these dynamics revealed their necessity for skilled action. Our work highlights that a complex pre-movement orchestration of coupling and decoupling ensures the selective engagement of relevant distributed networks to produce precise action.