Changes in Brain Activation during the Acquisition of a Multifrequency Bimanual Coordination Task: From the Cognitive Stage to Advanced Levels of Automaticity

Abstract

Little is known about activation changes reflecting overlearning, i.e., extensive motor training beyond asymptotic performance. Here we used functional magnetic resonance imaging to trace the neural shifts from an initial to a skilled (learning) and finally overlearned stage (automatization). Scanning occurred before training (PRE) and after 1 (MID) and 2 weeks (POST) of intensive practice on a new bimanual coordination task (Ͼ10,500 cycles). Kinematics revealed major improvements between PRE and MID sessions, whereas MID to POST session performance leveled off, indicative of learning and automatization, respectively. Imaging findings showed that activation decreased in bilateral opercular areas, bilateral ventrolateral prefrontal cortex, the right ventral premotor and supramarginal gyrus, and the anterior cingulate sulcus during the learning stage and in the supplementary motor area during the automatization stage. These changes are hypothesized to reflect decreases in attention-demanding sensory processing, as well as suppression of preferred coordination tendencies as a prelude to acquiring new coordination modes. Conversely, learning-related increases were observed in the primary motor cortex (M1), posterior cingulate zone (PCZ), putamen, and right anterior cerebellum. Importantly, both M1 and PCZ activation decreased again to initial level (PRE) during automated performance (POST). Only the putamen and anterior cerebellum remained more activated across both learning and automatization stages, supporting their crucial role in long-term motor memory formation for coordination tasks.

Cerebellar Plasticity and the Automation of First-Order Rules

“…jneurosci.org as supplemental material). Whereas previous studies have demonstrated such plasticity in the human cerebellum for motor learning (Imamizu et al, 2000(Imamizu et al, , 2003Ramnani et al, 2000;Ramnani and Passingham, 2001;Ungerleider et al, 2002;van Mier et al, 2004;Miall and Jenkinson, 2005;Penhune and Doyon, 2005;Puttemans et al, 2005), for the first time our study demonstrates plastic changes in cerebellar cortical parts of the "prefrontal loop" that occur as a direct consequence of manipulating the automaticity of rulebased information processing. Such activity reflects the acquisition of internal models of prefrontal information processing that contribute to the automatic execution of cognitive operations (Balsters and Ramnani, 2008).…”

“…These have been supported by empirical demonstrations of motor learning-related cerebellar plasticity using electrophysiology in nonhuman primates (Gilbert and Thach, 1977;Ojakangas and Ebner, 1992;Greger and Norris, 2005;Soetedjo and Fuchs, 2006;Medina and Lisberger, 2009) and numerous functional neuroimaging studies in humans (Friston et al, 1992;Imamizu et al, 2000Imamizu et al, , 2003Ramnani et al, 2000;Ramnani and Passingham, 2001;Ungerleider et al, 2002;van Mier et al, 2004;Miall and Jenkinson, 2005;Penhune and Doyon, 2005;Puttemans et al, 2005). Motor learning is likely to depend on information flow between cortical motor areas and cerebellar cortex via the pontine nuclei (Allen and Tsukahara, 1974;Wolpert and Kawato, 1998), and changes in the strength of synapses onto Purkinje cells (PCs; the principal computational units and output neurons of the cerebellar cortex).…”

Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

“…Nevertheless, our results suggest that this structure does not only reflect the consolidation of a newly learned sequence of movements (6,7,17,18), but that this physiological process is facilitated by sleep. Indeed, increases of activity within the striatum have previously been related to the acquisition of wrist movement sequences (19)(20)(21) per se, as well as the learning of MSL, as opposed to the mere increase in speed of finger movements (22). Moreover, such increase in striatal activity has also been seen following motor memory consolidation when sleep (10), or a 24-h delay including sleep is present after initial learning (23).…”

Exercise of mechanisms of dynamic stability improves the stability state after an unexpected gait perturbation in elderly

“…Further, the repeated application of the mechanisms of dynamic stability seems to facilitate the adequate use of those mechanisms even in unfamiliar situations in order to regain balance. This improvement may be ascribed to a shift from prefrontal activity to a subcortical circuit, involving the cerebellum and basal ganglia, accompanied by increased automatic performance (Floyer-Lea and Matthews 2004;Puttemans et al 2005;Taube et al 2007). Several exercise interventions have so far shown to be effective in reducing the risk of falls in older adults by means of balance, coordination, or strength training (for review see Gillespie et al 2010).…”