Lesions in supplementary motor area interfere with a monkey's performance of a bimanual coordination task

Brinkman, Cobie

doi:10.1016/0304-3940(81)90441-9

Cited by 163 publications

(57 citation statements)

References 10 publications

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“…The effect seen in the medial wall, comprising the posterior (behind the anterior commissure) SMA and a locus in the cingulate gyrus bilaterally, again is in accordance with results of previous nonparametric neuroimaging studies (24,30,31). SMA lesions have been shown to impair bimanual coordination (32,33).…”

Section: Discussionsupporting

confidence: 90%

Transitions between dynamical states of differing stability in the human brain

Meyer‐Lindenberg

Ziemann

Hajak

et al. 2002

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

170

130

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What mechanisms underlie the flexible formation, adaptation, synchronization, and dissolution of large-scale neural assemblies from the 10 10 densely interconnected, continuously active neurons of the human brain? Nonlinear dynamics provides a unifying perspective on self-organization. It shows that the emergence of patterns in open, nonequilibrium systems is governed by their stability in response to small disturbances and predicts macroscopic transitions between patterns of differing stability. Here, we directly demonstrate that such transitions can be elicited in the human brain by interference at the neural level. As a probe, we used a classic motor coordination paradigm exhibiting well described movement states of differing stability. Functional neuroimaging identified premotor (PMA) and supplementary motor (SMA) cortices as having neural activity linked to the degree of behavioral instability. These regions then were transiently disturbed with graded transcranial magnetic stimulation, which caused sustained and macroscopic behavioral transitions from the less stable out-of-phase to the stable in-phase movement, whereas the stable pattern could not be affected. Moreover, the strength of the disturbance needed (a measure of neural stability) was linked to the degree of behavioral stability, demonstrating the applicability of nonlinear system theory as a powerful predictor of the dynamical repertoire of the human brain.I maging of the living human brain routinely reveals patterns corresponding to the synchronized action of billions of neurons (1). The brain's formation of these large-scale distributed neural assemblies and the rapid transition between them is a striking example of self-organization. In complex systems far from equilibrium, nonlinear systems theory has proposed that the decisive parameter governing such collective emergent behavior is stability to small-scale disturbances; which dynamic patterns get selected from the vast array of possible combinations depends on their relative stability (2). Nonlinear systems exhibit pronounced susceptibility to small disturbances due to a hallmark property called ''sensitive dependence on initial conditions,'' meaning that minute changes to the system's state result in large-scale alterations.A further fundamental prediction of this approach is that self-organization depends on the occurrence of sudden macroscopic transitions between states of differing stability (usually called phase transitions; ref. 3). Therefore, if the presence of transitions between differentially stable patterns could be established, this would uncover a fundamental determinant of the dynamic repertoire of the central nervous system (4). Consequently, transition, synchronization and stability phenomena in neuronal membranes, cells, and small assemblies have been studied intensively (5-7). In humans, correlative evidence comes from the observation of electrophysiological changes as a consequence of alterations of stability in motor behavior, an area to which this theory has been applie...

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Section: Discussionsupporting

confidence: 90%

Transitions between dynamical states of differing stability in the human brain

Meyer‐Lindenberg

Ziemann

Hajak

et al. 2002

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

170

130

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“…This task, which involves a modification of the test board used by Brinkman (Brinkman 1981), was designed to test bimanual motor coordination, procedural learning and motivation to work for a preferred food reinforcer (raisins). Monkeys are easily trained on this task and reach a high level of proficiency.…”

Section: Bimanual Motor Skill Task (Bms)mentioning

confidence: 99%

Controlled and Behaviorally Relevant Levels of Oral Ethanol Intake in Rhesus Macaques Using a Flavorant‐Fade Procedure

Katner

Flynn

Huben

et al. 2004

Alcoholism Clin & Exp Res

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Background: Flavorant‐fading procedures can initiate and maintain oral ethanol intake in rodents. The present study developed a similar procedure to achieve controlled and behaviorally relevant levels of ethanol intake in monkeys.Methods: Male rhesus macaques (N= 13) were initially given the opportunity to consume 0.5 g/kg of a 1% (w/v) ethanol plus 4% (w/v) Tang solution in 1‐hr limited‐access sessions without the requirement of an operant response. Once consumption was stable at a particular concentration (%) and/or amount (g/kg), animals were given access to higher concentrations and/or amounts of ethanol. Animals were tested on a bimanual motor skill (BMS) task 20 and 90 min after consumption to assess behavioral impairment. Blood alcohol levels (BALs) were assessed after a session in which animals had the opportunity to consume up to 3.0 g/kg of 6% (w/v) ethanol.Results: The gradual fading up of higher concentrations and amounts of ethanol resulted in controlled and robust levels (>2.0 g/kg) of ethanol intake in half of the subjects. Increasing the concentration of the sweetener from 4 to 6% (w/v) was effective in initiating consumption in three animals. Two monkeys required the additional step of presenting the increased‐sweetener solutions after a meal (postprandial consumption) to initiate significant ethanol intake. Animals were significantly impaired on the BMS task after consumption of 2.0, 2.5, and 3.0 g/kg of ethanol. Individual consumption ranging from 0.8 to 3.0 g/kg of ethanol produced BALs of 18 to 269 mg/dl.Conclusions: The flavorant‐fading procedure was effective in producing behaviorally relevant levels of ethanol consumption in rhesus macaques. This model facilitated a randomized‐dose procedure to determine the behavioral effects of 0.5 to 3.0 g/kg of ethanol. This procedure therefore is of significant utility in determining behavioral or physiologic effects of specific doses of consumed ethanol in monkeys.

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“…Important roles for the medial wall motor areas in spatial bimanual coordination have been firmly established with a variety of techniques, including electrophysiological recordings (Brinkman and Porter 1979;Donchin et al 1998;Tanji et al 1987), lesion studies in nonhuman primates (Brinkman 1981(Brinkman , 1984 and humans (Bleasel et al 1996;Stephan et al 1999a), and neuroimaging recordings (Ehrsson et al 2000b;Goerres et al 1998;Sadato et al 1997;Stephan et al 1999a,b;Toyokura et al 1999). The SMA and preSMA have also been implicated in movement sequence control (see e.g., Sadato et al 1996;Tanji and Shima 1994), and in explicit timing functions (Halsband et al 1993;Ullén et al 2001).…”

Section: Polyrhythmic Coordinationmentioning

confidence: 99%

Rhythm and Beat Perception in Motor Areas of the Brain

Grahn¹,

Brett²

2007

Journal of Cognitive Neuroscience

831

872

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. Without practice, bimanual movements can typically be performed either in phase or in antiphase. Complex temporal coordination, e.g., during movements at different frequencies with a noninteger ratio (polyrhythms), requires training. Here, we investigate the organization of the neural control systems for in-phase, antiphase, and polyrhythmic coordination using functional magnetic resonance imaging (fMRI). Brisk rhythmic tapping with the index fingers was used as a model behavior. We demonstrate different patterns of brain activity during in-phase and antiphase coordination. In-phase coordination was characterized by activation of the right anterior cerebellum and cingulate motor area (CMA). Antiphase coordination was accompanied by extensive fronto-parieto-temporal activations, including the supplementary motor area (SMA), the preSMA, and the bilateral inferior parietal gyri, premotor cortex, and superior temporal gyri. When contrasting polyrhythmic tapping with in-phase tapping, activity was seen in the same set of brain regions, and in the posterior cerebellum and the CMA. Antiphase and polyrhythmic coordination may thus to a large extent use common neural control circuitry. In a separate experiment, we analyzed the neural control of the rhythmic structure and the serial order of finger movements during polyrhythmic tapping. Polyrhythmic tapping was compared with an isochronous coordination pattern that retained the same serial order of finger movements as the polyrhythm. This experiment showed that the preSMA and the bilateral superior temporal gyri may be crucial for the rhythmic control of polyrhythmic tapping, while the cerebellum, the CMA, and the premotor cortices presumably are more involved in the ordinal control of the sequence of finger movements.

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Lesions in supplementary motor area interfere with a monkey's performance of a bimanual coordination task

Cited by 163 publications

References 10 publications

Transitions between dynamical states of differing stability in the human brain

Transitions between dynamical states of differing stability in the human brain

Controlled and Behaviorally Relevant Levels of Oral Ethanol Intake in Rhesus Macaques Using a Flavorant‐Fade Procedure

Rhythm and Beat Perception in Motor Areas of the Brain

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