Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice

Abstract

The planning of goal-directed movements requires sensory, temporal, and contextual information to be combined. Sensorimotor functions are embedded in large neuronal networks, but it is unclear how networks organize their activity in space and time to optimize behavior. Temporal coordination of activity in many neurons within a network, e.g., spike synchrony, might be complementary to a firing rate code, allowing efficient computation with overall less population activity. Here we asked the question whether intensive practice induces long-term modifications in the temporal structure of synchrony and firing rate at the population level. Three monkeys were trained in a delayed pointing task in which the selection of movement direction depended on correct time estimation. The synchronous firing among pairs of simultaneously recorded neurons in motor cortex was analyzed using the "unitary event" technique. The evolution of synchrony in both time, within the trial, and temporal precision was then quantified at the level of an entire population of neurons by using two different quantification techniques and compared with the population firing rate. We find that the task timing was represented in the temporal structure of significant spike synchronization at the population level. During practice, the temporal structure of synchrony was shaped, with synchrony becoming stronger and more localized in time during late experimental sessions, in parallel with an improvement in behavioral performance. Concurrently, the average population firing rate mainly decreased. Performance optimization through practice might therefore be achieved by boosting the computational contribution of spike synchrony, allowing an overall reduction in population activity.

Computer simulations of synchrony and oscillations evoked by two coherent inputs

“…In contrast, for periodic patterns, STDP can suppress temporarily generated noisy spikes that have less temporal relations. This result is correspondent with the physiological experiment reports that the synchrony in the motor cortex becomes stronger and more localized in time with improvement of behavioral performance as the learning proceeds (Kilavik et al 2009). Taken together, periodic spatiotemporal patterns will be better than populational modulation as a method of information transmission in oscillatory waves.…”

“…Then it must be natural that both of modulated waves and spatiotemporal spikes are observed in the brain. The direct evidence of spatiotemporal patterns are few, but a transient synchrony such as ''unitary event'' has been reported (Kilavik et al 2009;Grammont and Riehle 2003). Some transient synchronies organized by cell assemblies (Singer 1999(Singer , 2009) may contribute to a transient spatiotemporal pattern.…”

“…Coherent oscillations have been reported in the motor related areas (Ohara et al 2001;Lee 2003Lee , 2004Hatsopoulos et al 1998;Grammont and Riehle 2003;Kilavik et al 2009) as well as the other cortical areas (Roelfsema et al 1997;Rodriguez et al 2004). For example, 20 to 30 Hz oscillations related to an action have been observed in the premotor cortical neurons (Lebedev and Wise 2000).…”

Evoked Potentials in Motor Cortical Local Field Potentials Reflect Task Timing and Behavioral Performance

“…This indicates that multiple processes are reflected in EP modulations, related to, on the one hand, trial-by-trial changes in network activity (see preceding text), possibly reflecting fluctuations in the level of attention and readiness and, on the other hand, long-term changes in network activity, reflecting repeated task practice (for studies of motor cortical spiking activity in relation to long-term task practice also see Kilavik et al 2009;Matsuzaka et al 2007;Schieber 2002). Most studies of motor cortical plasticity during motor learning were related to relatively short periods, concentrating on single sessions or a few days (for a review see Sanes and Donoghue 2000).…”

Differential Involvement of Excitatory and Inhibitory Neurons of Cat Motor Cortex in Coincident Spike Activity Related to Behavioral Context

“…Coincident firing activity in the motor cortex could be a marker of neural assembly formation related to representation and association of movement features. Many studies have investigated associations in spiking activity in the motor cortex (MI) and related it to shared involvement in a motor task, movement parameters, motor preparation, motor learning, and behavioral context of movement (Allum et al, 1982;Murphy et al, 1985a,b;Kwan et al, 1987;Smith and Fetz, 1989;Vaadia et al, 1995;Murthy and Fetz, 1996;Riehle et al, 1997Riehle et al, , 2000Donoghue et al, 1998;Lee et al, 1998;Baker et al, 2001;Grammont and Riehle, 2003;Jackson et al, 2003;Ghosh et al, 2009;Kilavik et al, 2009). However, coincident activity that is unrelated to movement tasks has also been observed in motor cortex (Murthy and Fetz, 1996;Riehle et al, 1997;Donoghue et al, 1998;Ghosh et al, 2009).…”