Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study (original) (raw)
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Presupplementary motor area activation during sequence learning reflects visuo-motor association
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1999
In preceding studies (Hikosaka et al., 1996; Sakai et al., 1998) we have shown that the presupplementary motor area (pre-SMA), an anterior part of the medial premotor cortex, is active during visuo-motor sequence learning. However, the paradigm required the subjects first to acquire correct visuo-motor association and then to acquire correct sequence, and it was still unknown which of the two processes the pre-SMA is involved in. To further characterize the role of pre-SMA, we have conducted another series of functional magnetic resonance imaging experiments using three learning paradigms. The three were the same in that they involved a visuo-motor association component, but they differed in terms of the involvement of sequential components; one involved no sequence learning, whereas the other two involved learning of motor sequence or perceptual sequence. Comparison of the learning conditions with the any-order button press condition revealed pre-SMA activation in all three paradig...
Transition of brain activation from frontal to parietal areas in visuomotor sequence learning
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1998
We studied the neural correlates of visuomotor sequence learning using functional magnetic resonance imaging (fMRI). In the test condition, subjects learned, by trial and error, the correct order of pressing two buttons consecutively for 10 pairs of buttons (2 x 10 task); in the control condition, they pressed buttons in any order. Comparison between the test condition and the control condition revealed four brain areas specifically related to learning: the dorsolateral prefrontal cortex (DLPFC), the presupplementary motor area (pre-SMA), the precuneus, and the intraparietal sulcus (IPS). We found that the time course of activation during learning was different between these areas. To normalize the individual differences in the speed of learning, we classified the performance of each subject into three learning stages: early, intermediate, and advanced stages. Both the relative increase of signal intensity and the number of activated pixels within the four areas showed significant c...
Neuronal Activity in Medial Frontal Cortex During Learning of Sequential Procedures
Journal of Neurophysiology, 1998
Nakamura, Kae, Katsuyuki Sakai, and Okihide Hikosaka. Neuronal activity in medial frontal cortex during learning of sequential procedures. J. Neurophysiol. 80: 2671–2687, 1998. To study the role of medial frontal cortex in learning and memory of sequential procedures, we examined neuronal activity of the presupplementary motor area (pre-SMA) and supplementary motor area (SMA) while monkeys ( n = 2) performed a sequential button press task, “2 × 5 task.” In this paradigm, 2 of 16 (4 × 4 matrix) light-emitting diode buttons (called “set”) were illuminated simultaneously and the monkey had to press them in a predetermined order. A total of five sets (called “hyperset”) was presented in a fixed order for completion of a trial. We examined the neuronal activity of each cell using two kinds of hypersets: new hypersets that the monkey experienced for the first time for which he had to find the correct orders of button presses by trial-and-error and learned hypersets that the monkey had lea...
Anatomy of motor learning. I. Frontal cortex and attention to action
Journal of neurophysiology, 1997
We used positron emission tomography to study new learning and automatic performance in normal volunteers. Subjects learned sequences of eight finger movements by trial and error. In a previous experiment we showed that the prefrontal cortex was activated during new learning but not during during automatic performance. The aim of the present experiment was to see what areas could be reactivated if the subjects performed the prelearned sequence but were required to pay attention to what they were doing. Scans were carried out under four conditions. In the first the subjects performed a prelearned sequence of eight key presses; this sequence was learned before scanning and was practiced until it had become overlearned, so that the subjects were able to perform it automatically. In the second condition the subjects learned a new sequence during scanning. In a third condition the subjects performed the prelearned sequence, but they were required to attend to what they were doing; they w...
Neuroscience, 2011
A broad range of motor skills, such as speech and writing, evolves with the ability to articulate elementary motor movements into novel sequences that come to be performed smoothly through practice. Neuroimaging studies in humans have demonstrated the involvement of the cerebello-cortical and striato-cortical motor loops in the course of motor sequence learning. Nonetheless, the nature of the improvement and brain mechanisms underlying different parameters of movement kinematics are not yet fully ascertained. We aimed at dissociating the cerebral substrates related to the increase in performance on two kinematic indices: velocity, that is the speed with which each single movement in the sequence is produced, and transitions, that is the duration of the gap between these individual movements. In this event-related fMRI experiment, participants practiced an eight-element sequence of finger presses on a keypad which allowed to record those kinematic movement parameters. Velocity was associated with activations in the ipsilateral spinocerebellum (lobules 4-5, 8 and medial lobule 6) and in the contralateral primary motor cortex. Transitions were associated with increased activity in the neocerebellum (lobules 6 bilaterally and lobule 4-5 ipsilaterally), as well as with activations within the right and left putamen and a broader bilateral network of motor cortical areas. These findings indicate that, rather than being the product of a single mechanism, the general improvement in motor performance associated with early motor sequence learning arises from at least two distinct kinematic processes, whose behavioral expressions are supported by partially overlapping and segregated brain networks.
Specialized Neural Systems Underlying Representations of Sequential Movements
Journal of Cognitive Neuroscience, 2000
The ease by which movements are combined into skilled actions depends on many factors, including the complexity of movement sequences. Complexity can be defined by the surface structure of a sequence, including motoric properties such as the types of effectors, and by the abstract or sequence-specific structure, which is apparent in the relations amongst movements, such as repetitions. It is not known whether different neural systems support the cognitive and the sensorimotor processes underlying different structural properties of sequential actions. We investigated this question using whole-brain functional magnetic resonance imaging (fMRI) in healthy adults as they performed sequences of five key presses involving up to three fingers. The structure of sequences was defined by two factors that independently lengthen the time to plan sequences before movement: the number of different fingers (1-3; surface structure) and the number of finger transitions (0-4; sequence-specific structure). The results showed that systems involved in visual processing (extrastriate cortex) and the preparation of sensory aspects of movement (rostral inferior parietal and ventral premotor cortex (PMv)) correlated with both properties of sequence structure. The number of different fingers positively correlated with activation intensity in the cerebellum and superior parietal cortex (anterior), systems associated with sensorimotor, and kinematic representations of movement, respectively. The number of finger transitions correlated with activation in systems previously associated with sequence-specific processing, including the inferior parietal and the dorsal premotor cortex (PMd), and in interconnecting superior temporal-middle frontal gyrus networks. Different patterns of activation in the left and right inferior parietal cortex were associated with different sequences, consistent with the speculation that sequences are encoded using different mnemonics, depending on the sequence-specific structure. In contrast, PMd activation correlated positively with increases in the number of transitions, consistent with the role of this area in the retrieval or preparation of abstract action plans. These findings suggest that the surface and the sequence-specific structure of sequential movements can be distinguished by distinct distributed systems that support their underlying mental operations.
Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study
Brain, 1998
We examined the dynamic involvement of different brain regions in implicit and explicit motor sequence learning using PET. In a serial reaction time task, subjects pressed each of four buttons with a different finger of the right hand in response to a visually presented number. Test sessions consisted of 10 cycles of the same 10-item sequence. The effects of explicit and implicit learning were assessed separately using a different behavioural parameter for each type of learning: correct recall of the test sequence for explicit learning and improvement of reaction time before the successful recall of any component of the test sequence for implicit learning. Regional cerebral blood flow was measured repeatedly during the task, and a parametric analysis was performed to identify brain regions in which activity was significantly correlated with subjects' performances: i.e. with correct recall of the test sequence or with reaction time. Explicit learning, shown as a positive correlation with the correct recall of the sequence, was associated with increased activity in Abbreviations: PRE ϭ training block; rCBF ϭ regional CBF; RND ϭ random condition block; SEQ ϭ sequence condition block; SMA ϭ supplementary motor area; SM1 ϭ primary sensorimotor cortex; SRTT ϭ serial reaction time task; VIS ϭ visual control condition block © Oxford University Press 1998 the posterior parietal cortex, precuneus and premotor cortex bilaterally, also in the supplementary motor area (SMA) predominantly in the left anterior part, left thalamus, and right dorsolateral prefrontal cortex. In contrast, the reaction time showed a different pattern of correlation during different learning phases. During the implicit learning phase, when the subjects were not aware of the sequence, improvement of the reaction time was associated with increased activity in the contralateral primary sensorimotor cortex (SM1). During the explicit learning phase, the reaction time was significantly correlated with activity in a part of the frontoparietal network. During the post-learning phase, when the subjects achieved all components of the sequence explicitly, the reaction time was correlated with the activity in the ipsilateral SM1 and posterior part of the SMA. These results show that different sets of cortical regions are dynamically involved in implicit and explicit motor sequence learning.
The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study
NeuroImage, 1998
There is a discrepancy between the results of imaging studies in which subjects learn motor sequences. Some experiments have shown decreases in the activation of some areas as learning increased, whereas others have reported learning-related increases as learning progressed. We have exploited fMRI to measure changes in blood oxygen level-dependent (BOLD) signal throughout the course of learning. T2*-weighted echo-planar images were acquired over the whole brain for 40 min while the subjects learned a sequence eight moves long by trial and error. The movements were visually paced every 3.2 s and visual feedback was provided to the subjects. A baseline period followed each activation period. The effect due to the experimental conditions was modeled using a squarewave function, time locked to their occurrence. Changes over time in the difference between activation and baseline signal were modeled using a set of polynomial basis functions. This allowed us to take into account linear as well as nonlinear changes over time. Low-frequency changes over time common to both activation and baseline conditions (and thus not learning related) were modeled and removed. Linear and nonlinear changes of BOLD signal over time were found in prefrontal, premotor, and parietal cortex and in neostriatal and cerebellar areas. Single-unit recordings in nonhuman primates during the learning of motor tasks have clearly shown increased activity early in learning, followed by a decrease as learning progressed. Both phenomena can be observed at the population level in the present study. 1998 Academic Press
Brain activation during execution and motor imagery of novel and skilled sequential hand movements
NeuroImage, 2005
This experiment used functional magnetic resonance imaging (fMRI) to compare functional neuroanatomy associated with executed and imagined hand movements in novel and skilled learning phases. We hypothesized that 1 week of intensive physical practice would strengthen the motor representation of a hand motor sequence and increase the similarity of functional neuroanatomy associated with executed and imagined hand movements. During fMRI scanning, a right-hand self-paced button press sequence was executed and imagined before (NOVEL) and after (SKILLED) 1 week of intensive physical practice (n = 54; right-hand dominant). The mean execution rate was significantly faster in the SKILLED (3.8 Hz) than the NOVEL condition (2.5 Hz) (P < 0.001), but there was no difference in execution errors. Activation foci associated with execution and imagery was congruent in both the NOVEL and SKILLED conditions, though activation features were more similar in the SKILLED versus NOVEL phase. In the NOVEL phase, activations were more extensive during execution than imagery in primary and secondary cortical motor volumes and the cerebellum, while during imagery activations were greater in the striatum. In the SKILLED phase, activation features within these same volumes became increasingly similar for execution and imagery, though imagery more heavily activated premotor areas, inferior parietal lobe, and medial temporal lobe, while execution more heavily activated the precentral/postcentral gyri, striatum, and cerebellum. This experiment demonstrated congruent activation of the cortical and subcortical motor system during both novel and skilled learning phases, supporting the effectiveness of motor imagery-based mental practice techniques for both the acquisition of new skills and the rehearsal of skilled movements. D