Emergence of reproducible spatiotemporal activity during motor learning

Abstract

The motor cortex is capable of reliably driving complex movements yet exhibits considerable plasticity during motor learning. These observations suggest that the fundamental relationship between motor cortex activity and movement may not be fixed but is instead shaped by learning; however, to what extent and how motor learning shapes this relationship are not fully understood. Here we addressed this issue by using in vivo two-photon calcium imaging to monitor the activity of the same population of hundreds of layer 2/3 neurons while mice learned a forelimb lever-press task over two weeks. Excitatory and inhibitory neurons were identified by transgenic labelling. Inhibitory neuron activity was relatively stable and balanced local excitatory neuron activity on a movement-by-movement basis, whereas excitatory neuron activity showed higher dynamism during the initial phase of learning. The dynamics of excitatory neurons during the initial phase involved the expansion of the movement-related population which explored various activity patterns even during similar movements. This was followed by a refinement into a smaller population exhibiting reproducible spatiotemporal sequences of activity. This pattern of activity associated with the learned movement was unique to expert animals and not observed during similar movements made during the naive phase, and the relationship between neuronal activity and individual movements became more consistent with learning. These changes in population activity coincided with a transient increase in dendritic spine turnover in these neurons. Our results indicate that a novel and reproducible activity-movement relationship develops as a result of motor learning, and we speculate that synaptic plasticity within the motor cortex underlies the emergence of reproducible spatiotemporal activity patterns for learned movements. These results underscore the profound influence of learning on the way that the cortex produces movements.

Stroke and the Connectome: How Connectivity Guides Therapeutic Intervention

“…Although turnover was specific to the peri-infarct zone, it is possible that these studies were not sufficiently sensitive to resolve structural rearrangements involving a relatively small fraction of the total inputs to a distant area in the background of many unchanged connections. Recent data in noninjured animals support the proposal that motor learning is achieved through long-lasting changes in dendritic spine turnover and the fine-tuning of individual neuron responsiveness in motor cortex (Peters et al, 2014;Xu et al, 2009). It is conceivable that physiological factors known to regulate structural plasticity during motor learning in normal animals, such as sleep (Yang et al, 2014), may provide insight into how to modulate recovery within the poststroke brain.…”

Patterns of Modulation in the Activity and Connectivity of Motor Cortex during the Repeated Generation of Movement Sequences

“…These modulations, during the performance of the U-FOS but not the T-FOS, presumably reflect the short-term accumulation of experience with the novel order (sequence, syntax) of movements as both sequences were composed of the same component opposition movements. It has been shown that the initial phases of motor task acquisition are characterized by various activity patterns of movement-related neurons selected and engaged from a more extensive pool in motor cortex; these activity patterns stabilize and a more restricted population is consistently engaged after extensive training (Peters et al, 2014). The transient stabilization of neural activity upon repeated performance blocks, in the current study, may result from the selection of a particular subset of excitatory neurons that were "tried out" during the corresponding initial blocks.…”

“…There is evidence suggesting that lower-level motor areas, including M1, not only generate the pattern of muscle activity necessary to implement action plans but may also play an active role in both the acquisition and retention of complex motor skills in mammalian brains (Peters, Chen, & Komiyama, 2014;Yang et al, 2014;Xu et al, 2009;Yang, Pan, & Gan, 2009;Matsuzaka, Picard, & Strick, 2007;Ben-Shaul et al, 2004;Kleim et al, 2004;Carpenter et al, 1999;Nudo et al, 1996). Animal studies indicate that practice on a motor task may lead to rapid, but long-lasting, synaptic reorganization in M1 ( Yang et al, 2009( Yang et al, , 2014Xu et al, 2009).…”

Nowhere and Everywhere: The Causal Origin of Voluntary Action

“…Other recent data reveals the emergence of stable patterns of neural activity in rodent M1 for cued movements (Peters et al 2014), which might at first seem inconsistent with the argument above. But bear in mind that these patterns were observed in M1, where activity-pattern-to-behavior pairings are likely to be much more constrained than in premotor or other areas of cortex.…”

“…Indeed Peters found that during learning the system Bexplored various activity patterns even during similar movements^ (Peters et al 2014, p. 263). Thus, even if highly reproducible patterns may emerge in primary motor cortex for well-learned cued movements, it seems clear from these two recent studies (Peters et al 2014;Vogelstein et al 2014) that it is possible for very different patterns of neural activity to lead to the very same movement, even at very late stages of motor control (as in M1).…”