Differential Cortical and Subcortical Activations in Learning Rotations and Gains for Reaching: A PET Study

Abstract

. Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. J Neurophysiol 91: 924 -933, 2004. First published October 1, 2003 10.1152/jn.00675.2003. Previous studies suggest that horizontal reaching movements are planned vectorially with independent specification of direction and extent. The transformation from visual to hand-centered coordinates requires the learning of a task-specific reference frame and scaling factor. We studied learning of a novel reference frame by imposing a screencursor rotation and learning of a scaling factor by imposing a novel gain. Previous work demonstrates that rotation and gain learning have different time courses and patterns of generalization. Here we used PET to identify and compare brain areas activated during rotation and gain learning, with a baseline motor-execution task as the subtracted control. Previous work has shown that the time courses of rotation and gain adaptation have a short rapid phase followed by a longer slow phase. We therefore also sought to compare activations associated with the rapid and slower phases of adaptation. We isolated the rapid phase by alternating opposite values of the rotation or gain every 16 movements. The rapid phase of rotation adaptation activated the preSMA. More complete adaptation to the rotation activated right ventral premotor cortex, right posterior parietal cortex, and the left lateral cerebellum. The rapid phase of gain learning only activated subcortical structures: bilateral putamen and left cerebellum. More complete gain learning failed to show any significant activation. We conclude that the time course of rotation adaptation is paralleled by a frontoparietal shift in activated cortical regions. In contrast, early gain adaptation involves only subcortical structures, which we suggest reflects a more automatic process of contextual recalibration of a scaling factor.

Basal ganglia network mediates the control of movement amplitude

“…4). A similar pattern of bilateral basal ganglia activation has been observed in recent imaging studies of brain activity correlated with the extent and velocity of arm movement and with alterations in the`gain' for movement extent and velocity (Krakauer et al, 2004). These regions of the striatum receive strong bilateral input from motor and premotor cortices (Flaherty & Graybiel, 1991;Takada et al, 1998) and are considered part of the basal ganglia skeletomotor circuit (Alexander et al, 1990).…”

“…Relevant here, precues for movement extent and direction can reduce RTs additively, implying thereby that movement direction and amplitude are planned separately (Rosenbaum, 1980;Lepine et al, 1989;Bock & Arnold, 1992). This idea is also supported by disparate additional observations: speci®cation of extent and direction follows different timecourses (Ghez et al, 1997); visuomotor gains are learnt more readily and generalize more widely than directional rotations (Krakauer et al, 2000;Vindras & Viviani, 2002); learning of rotations and gains activates different cortical and subcortical networks (Krakauer et al, 2004); and, direction and extent errors vary independently (Gordon et al, 1994;Desmurget et al, 1997;Vindras & Viviani, 1998;Desmurget et al, 1999). This perspective should not be taken to imply that extent is controlled in isolation, but rather that, at certain stages of motor planning, a constellation of parameters related to the extent of movement are controlled independently from parameters related to movement direction.…”

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

“…In the context of brain stimulation and localization, the distinction between adaptation and skill is particularly important because they appear to be mediated by separate neural substrates. For example, finger-tapping skill tasks typically show learning-related activation in contralateral M1 (22,31), whereas adaptation tasks, such as visuomotor rotation, predominantly activate posterior parietal cortex and cerebellum (32)(33)(34).…”

Long-Term Retention Explained by a Model of Short-Term Learning in the Adaptive Control of Reaching

“…During learning, when TMS was applied over the posterior parietal cortex, the initial rapid adaptation was unaffected, whereas the later gradual increase in learning was significantly reduced. Recently, imaging techniques have been used to identify the neural networks associated with the different time courses of learning during motor adaptation (Krakauer et al 2004;Tunik et al 2007). Together these results suggest that subcomponents of the learning process with different learning rates may be attributed to particular neural areas and opens the possibility that these areas may be manipulated to impair or enhance the formation of long-term motor memories.…”