Strong neuron-to-body coupling implies weak neuron-to-neuron coupling in motor cortex

Abstract

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.

Changing phase relationship of the stepping rhythm to neuronal oscillatory theta activity in the septo-hippocampal network of mice

“…c Phase histograms of two medial septal rhythmic neurons simultaneously recorded during theta (top) and stepping (bottom) cycles (data are duplicated to illustrate rhythmicity) that separate populations of medial septal cells specialized to coordinate theta rhythmic population activity and stepping related locomotor activity in the navigation system. This can be interpreted in concert with a recent observation in motor cortical neurons, where strong neuron to population coupling implied weak neuron to body-movement coupling (Kells et al 2019). From an evolutionary perspective, body movement variables may provide temporal windows for synchronizing neural computations in body-relevant timescales, crucial for behavior.…”

Reduced complexity of brain and behavior due to MeCP2 disruption and excessive inhibition

“…Similarly, application of muscimol resulted in a large increase in synchrony for both normal and RTT rats. This result is somewhat surprising considering that stronger inhibition is often associated with reduced synchrony in theory 13,33 and GABA agonists can result in reduced synchrony 14 , but our finding is consistent with a recent study that applied muscimol in motor cortex of awake rats 7 .…”

“…Precisely how much and what kind of synchrony is best for motor coding and how motor function depends on changes in synchrony is poorly understood. Previous studies have shown that significant synchrony and correlations exist among neurons in motor cortex [4][5][6][7] . Is this coordinated activity beneficial or is it actually limiting the motor code?…”

“…Is this coordinated activity beneficial or is it actually limiting the motor code? Recent experiments have shown that correlations can limit motor coding 8 and that the neurons with strongest correlations in M1 are weakly related to body movements 7 . Nonetheless, most studies of synchrony or correlations among neurons in motor cortex have focused on how such coordinated activity may play a beneficial role in motor coding [9][10][11][12] .…”

“…For instance, many computational models suggest that synchrony is strongly dependent on E/I interactions [13][14][15][16] . Likewise, in experiments, pharmacological manipulation of E/I causes changes in synchrony 7,14,17 and the excessive synchrony that occurs during epileptic seizures is often attributed to an E/I imbalance 18,19 . Similarly, the majority of people with RTT suffer from seizures and many previous studies establish E/I imbalance as a common problem in RTT 20 .…”