Functional organization of human supplementary motor cortex studied by electrical stimulation

Fried, Itzhak; Katz, Amiram; McCarthy, Gregory; Sass, KJ; Williamson, Pétér D.; Spencer, S. S.; Spencer, D. D.

doi:10.1523/jneurosci.11-11-03656.1991

Cited by 677 publications

(411 citation statements)

References 33 publications

(47 reference statements)

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“…Our results are consistent with previous studies demonstrating that the medial PFC is necessary for motor inhibition (4,9,16,17). In monkeys, microstimulation of the supplementary eye field within the medial prefrontal cortex improved performance on an oculomotor version of the SST by delaying saccade inhibition (9), and stimulation of the pre-SMA inhibited automatic unwanted actions while facilitating a desired alternative (10).…”

Section: Discussionsupporting

confidence: 92%

Distinct frontal systems for response inhibition, attentional capture, and error processing

Sharp

Bonnelle

Boissezon

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

482

464

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Stopping an action in response to an unexpected event requires both that the event is attended to, and that the action is inhibited. Previous neuroimaging investigations of stopping have failed to adequately separate these cognitive elements. Here we used a version of the widely used Stop Signal Task that controls for the attentional capture of stop signals. This allowed us to fractionate the contributions of frontal regions, including the right inferior frontal gyrus and medial frontal cortex, to attentional capture, response inhibition, and error processing. A ventral attentional system, including the right inferior frontal gyrus, has been shown to respond to unexpected stimuli. In line with this evidence, we reasoned that lateral frontal regions support attentional capture, whereas medial frontal regions, including the presupplementary motor area (pre-SMA), actually inhibit the ongoing action. We tested this hypothesis by contrasting the brain networks associated with the presentation of unexpected stimuli against those associated with outright stopping. Functional MRI images were obtained in 26 healthy volunteers. Successful stopping was associated with activation of the right inferior frontal gyrus, as well as the pre-SMA. However, only activation of the pre-SMA differentiated stopping from a high-level baseline that controlled for attentional capture. As expected, unsuccessful attempts at stopping activated the anterior cingulate cortex. In keeping with work in nonhuman primates these findings demonstrate that successful motor inhibition is specifically associated with pre-SMA activation.attention | functional MRI | presupplementary motor area | stop signal task | stopping T he control of voluntary action depends critically upon the ability to inhibit unwanted responses. This process has been extensively studied using the Stop Signal Task (SST) (1). Previous work with this task provides evidence that both medial frontal regions, including the presupplementary motor area (pre-SMA), and more lateral regions, including the right inferior frontal gyrus (IFG; rIFG) and insula (Ins), are involved in stopping. However, the specific contributions of these regions to motor control are unresolved (2-4). Many functional imaging studies have demonstrated activation of right inferior frontal regions during stopping (2, 5-8) and individual differences in response inhibition correlate with the magnitude of the IFG/Ins activation during the SST (5). Activation of medial prefrontal regions are also observed during stopping (2, 5). Pre-SMA activation is correlated with the efficiency of inhibitory processing (2), and work in nonhuman primates supports a role for the medial prefrontal regions in behavioral inhibition (9, 10). Neuropsychological studies provide discrepant results, with correlations between the extent of damage and impairments of inhibitory function reported for both the right lateral and medial frontal regions (3, 4).A limitation of much of the previous neuroimaging literature is that "stop trials" conflate p...

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Section: Discussionsupporting

confidence: 92%

Distinct frontal systems for response inhibition, attentional capture, and error processing

Sharp

Bonnelle

Boissezon

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

482

464

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“…The peaks of activity lay in the SMA and pre-SMA. It is of interest that electrical stimulation of SMA in humans induces an urge to move limbs (19), and the BOLD signal in the pre-SMA increases when participants are asked to attend to the urge to produce a finger movement (20). Furthermore, activity in the SMA and pre-SMA increases before voluntary movement, reflecting the preparation to move (21)(22)(23)(24)(25).…”

Section: Discussionmentioning

confidence: 99%

“…Nineteen right-handed, healthy participants took part in the imaging experiments (11 males; all aged [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33]. Participation was limited to subjects who felt the rubber-hand illusion in preliminary testing; 9 other subjects were not scanned because they did not experience the illusion (see Prescanning Testing Phase in SI Text).…”

Section: Methodsmentioning

confidence: 99%

Threatening a rubber hand that you feel is yours elicits a cortical anxiety response

Ehrsson

Wiech

Weiskopf

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

344

293

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The feeling of body ownership is a fundamental aspect of selfconsciousness. The underlying neural mechanisms can be studied by using the illusion where a person is made to feel that a rubber hand is his or her own hand by brushing the person's hidden real hand and synchronously brushing the artificial hand that is in full view. Here we show that threat to the rubber hand can induce a similar level of activity in the brain areas associated with anxiety and interoceptive awareness (insula and anterior cingulate cortex) as when the person's real hand is threatened. We further show that the stronger the feeling of ownership of the artificial hand, the stronger the threat-evoked neuronal responses in the areas reflecting anxiety. Furthermore, across subjects, activity in multisensory areas reflecting ownership predicted the activity in the interoceptive system when the hand was under threat. Finally, we show that there is activity in medial wall motor areas, reflecting an urge to withdraw the artificial hand when it is under threat. These findings suggest that artificial limbs can evoke the same feelings as real limbs and provide objective neurophysiological evidence that the rubber hand is fully incorporated into the body. These findings are of fundamental importance because they suggest that the feeling of body ownership is associated with changes in the interoceptive systems.body image ͉ emotion ͉ fMRI ͉ multisensory ͉ self

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“…Fried et el. [19] observed large differences of stimulus effects in the rostral and caudal portions of the mesial frontal cortex. Only in the rostral part of stimulus sites did they elicit 'urge' in the subjects to initiate movements.…”

mentioning

confidence: 85%

Comparison of neuronal activity in the supplementary motor area and primary motor cortex

Tanji

Mushiake

1996

Cognitive Brain Research

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Neuronal activity in the supplementary motor area (SMA) and primary motor cortex (MI) have been compared in many experiments during performance of many different motor tasks. On one hand, the activity in both areas may appear similar, especially when the motor task is simple. On the other hand, if the motor tasks are more demanding, neuronal activity in the SMA exhibits a variety of complex relationship to many different aspects of motor behavior, while the activity in MI is mostly related to execution of motor task itself. Of particular interest is the neuronal activity in the SMA during preparation and execution of motor tasks when no external cues for the retrieval of appropriate motor act is available. Temporal sequencing of multiple movements is a typical example of the kind of motor task that requires profound activity in the SMA.Keywords: Supplementary motor area (SMA); Primary motor cortex (MI); Pre-SMA; Motor preparation; Motor sequence; Subhuman primate New concepts of motor areas in the medial frontal cortexUntil recently, only one motor representation area was known to exist in the medial part of the frontal lobe, as described in classical reports [55,80]. However, it is now proposed that at least four somatomotor fields and one oculomotor field exist in the medial frontal cortex. [65]. Traditionally, the supplementary motor area (SMA) has been defined as a single motor area in the frontal agranular cortex, corresponding to medial part of Brodmann's area 6. However, some indications for possible existence of heterogeneity in this region has been obtained [2,15,25,42]. On the basis of cytoarchitectonic analysis combined with cytochrome oxidase histochemistry and detailed ICMS studies, Rizzolatti and coworkers proposed a view that two motor areas exist in the region of the cortex traditionally defined as the SMA [41,44]. They termed the rostral and caudal areas as F6 and F3, largely corresponding to 6ab and 6aa of Vogts [78]. They also reported the existence of neuronal activity characteristic in mesial 6ab, namely, the activity during arm reaching-grasping movements [57]. Systematic attempts were made in our laboratory to determine whether it is possible to define two different areas unequivocally by a battery of physiological tests [45]. By implanting electrodes into the forelimb area of the MI, we found that field and unitary responses to electrical stimulation were distinct in the caudal part of mesial area 6, but not in the rostral part. The caudal part was distinctly more microexcitable by the ICMS than the rostral part. Neuronal responses to visual stimuli prevailed in the rostral part, but somatosensory responses were rare. The opposite was true in the caudal part [24,79]. Furthermore, single-unit activity during performance of a trained motor task was quantitatively analyzed and compared in the same individuals. Phasic responses to visual cue signals indicating the direction of forthcoming arm-reaching movement were more abundant in the rostral part. Neuronal activity changes during th...

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Functional organization of human supplementary motor cortex studied by electrical stimulation

Cited by 677 publications

References 33 publications

Distinct frontal systems for response inhibition, attentional capture, and error processing

Distinct frontal systems for response inhibition, attentional capture, and error processing

Threatening a rubber hand that you feel is yours elicits a cortical anxiety response

Comparison of neuronal activity in the supplementary motor area and primary motor cortex

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