fMRI investigation of cortical and subcortical networks in the learning of abstract and effector-specific representations of motor sequences

Abstract

AcknowledgmentsThis study was supported by grants from Japan Science and Technology Corporation under the ERATO and CREST schemes. We thank Richard Henson, Okihide Hikosaka, Hiroshi Imamizu, Mitsuo Kawato, and Hiroyuki Nakahara for helpful comments and Alex Harner for the experimental software. We thank anonymous reviewers for their suggestions for improving the manuscript. We thank Joe Gati, for the help in running the experiments and V. S. Chandrasekhar Pammi and Ahmed, UH for help with analysis. ABSTRACTA visuomotor sequence can be learned as a series of visuo-spatial cues or as a sequence of effector movements. Earlier imaging studies have revealed that a network of brain areas is activated in the course of motor sequence learning. However these studies do not address the question of the type of representation being established at various stages of visuomotor sequence learning. In an earlier behavioral study, we demonstrated that acquisition of visuo-spatial sequence representation enables rapid learning in the early stage and progressive establishment of somato-motor representation helps speedier execution by the late stage. We conducted functional magnetic resonance imaging (fMRI) experiments wherein subjects learned and practiced the same sequence alternately in normal and rotated settings. In one rotated setting (visual), subjects learned a new motor sequence in response to an identical sequence of visual cues as in normal. In another rotated setting (motor), the display sequence was altered as compared to normal, but the same sequence of effector movements were used to perform the sequence. Comparison of different rotated settings revealed analogous transitions both in the cortical and subcortical sites during visuomotor sequence learning  a transition of activity from parietal to parietalpremotor and then to premotor cortex and a concomitant shift was observed from anterior putamen to a combined activity in both anterior and posterior putamen and finally to posterior putamen. These results suggest a putative role for engagement of different cortical and subcortical networks at various stages of learning in supporting distinct sequence representations.

Evidence for a distributed hierarchy of action representation in the brain

“…Depending on training conditions, it is possible to demonstrate that participants are learning the perceptual ordering of stimuli in the task, the discrete motor responses in the task, or the outcome of the responses, that is, the distal goals or consequences of the action (Bapi, Doya, & Harner, 2000;Hazeltine, 2002). With SRT sequence learning there is typically increasing activity in supplementary motor area (SMA) or pre-supplementary motor area (pre-SMA) and the inferior parietal lobule (IPL) (Bapi, Miyapuram, Graydon, & Doya, 2006;Bischoff-Grethe, Goedert, Willingham, & Grafton, 2004;Grafton et al, 1995;Grafton, Hazeltine, & Ivry, 1998). At a single neuron level, coding for sequence order in a very small set of over-learned movements is observed in SMA in humans (Amador & Fried, 2004) and in monkeys within SMA, pre-SMA (Tanji, 1996;Tanji & Shima, 1994) and IPL as well as the motor cortex (Lu & Ashe, 2005) but not in regions associated with reaching (Batista & Andersen, 2001).…”

Evidence of Neuromuscular Adaptation According to Motor Sequential Learning in the Serial Reaction Time Task

“…It plays a critical role in adapting to changes in the physical environment in our daily lives 1) . On account of universality of the motor skill learning, investigators from many fields of neuroscience have attempted to define more precisely the factors and mechanisms associated with motor skill learning [2][3][4][5][6] . For evaluating the extent of motor skill learning, a variety of motor tasks have been used such as the target acquisition task, the tracking task, the serial reaction time ( S R T ) t a s k , e t c .…”

Changes in Cerebral and Cerebellar Activation Patterns Induced by Short-term Sequence Learning of a Serial Reaction Time Task: an fMRI Study

“…A considerable decrement in RT had occurred at the end of the two-week period of training and this is consistent with the acquisition of explicit knowledge [11][12][13] . A largescale motor network, including the frontal and parietal lobes and the cerebellum, which functions during learning of a task, has been reported in sequential learning studies of patterns of brain activation 4,14,15) . Our present findings showing the activation of bilateral SM1, PFC, PMA, posterior parietal lobes, and cerebellum, are consistent with prior findings of studies exploring brain activity concurrent with performance of sequence movement.…”

“…Effects of motor skill learning have been reported for a variety of motor tasks, including the serial reaction time (SRT) task, target acquisition task, tracking task, and so forth 2,3) . Recently, using the SRT task, many investigators have attempted to reveal more precisely the factors and mechanisms associated with specific effectors during learning 4,5) .…”