Function of striatum beyond inhibition and execution of motor responses

We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that whe...

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Published inHuman brain mapping Vol. 25; no. 3; pp. 336 - 344
Main Authors Vink, Matthijs, Kahn, René S., Raemaekers, Mathijs, van den Heuvel, Martijn, Boersma, Maria, Ramsey, Nick F.
Format Journal Article
LanguageEnglish
Published Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.07.2005
Wiley-Liss
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ISSN1065-9471
1097-0193
DOI10.1002/hbm.20111

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Abstract We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses. Hum Brain Mapp, 2005. © 2005 Wiley‐Liss, Inc.
AbstractList We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses. Hum Brain Mapp, 2005.
We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses.
We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses.We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses.
We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to designated items (STOP trials) within a similar series of motor stimuli. Striatal activation was increased significantly compared to that when responding to all targets within a series of motor stimuli, indicating that the striatum is more active when inhibitory motor control over responses is required. The likelihood of a STOP trial was varied parametrically by varying the number of GO trials before a STOP trial. We could thus measure the effect of expecting a STOP trial on the fMRI response in the striatum. We show for the first time in humans that the striatum becomes more active when the likelihood of inhibiting a planned motor response increases. Our findings suggest that the striatum is critically involved in inhibitory motor control, most likely by controlling the execution of planned motor responses. Hum Brain Mapp, 2005. © 2005 Wiley‐Liss, Inc.
Author van den Heuvel, Martijn
Ramsey, Nick F.
Boersma, Maria
Kahn, René S.
Vink, Matthijs
Raemaekers, Mathijs
AuthorAffiliation 1 Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
AuthorAffiliation_xml – name: 1 Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
Author_xml – sequence: 1
  givenname: Matthijs
  surname: Vink
  fullname: Vink, Matthijs
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– sequence: 2
  givenname: René S.
  surname: Kahn
  fullname: Kahn, René S.
  organization: Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
– sequence: 3
  givenname: Mathijs
  surname: Raemaekers
  fullname: Raemaekers, Mathijs
  organization: Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
– sequence: 4
  givenname: Martijn
  surname: van den Heuvel
  fullname: van den Heuvel, Martijn
  organization: Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
– sequence: 5
  givenname: Maria
  surname: Boersma
  fullname: Boersma, Maria
  organization: Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
– sequence: 6
  givenname: Nick F.
  surname: Ramsey
  fullname: Ramsey, Nick F.
  organization: Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, Department of Psychiatry, Heidelberglaan Utrecht, The Netherlands
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Issue 3
Keywords Nervous system diseases
basal ganglia
Radiodiagnosis
motor behavior
Central nervous system
inhibition
Corpus striatum
Basal ganglion
Nuclear magnetic resonance imaging
Encephalon
fMRI
striatum
Behavior
functional magnetic resonance imaging
Functional imaging
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
CC BY 4.0
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PMID 15852388
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PublicationDate July 2005
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  text: July 2005
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PublicationPlace Hoboken
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PublicationTitle Human brain mapping
PublicationTitleAlternate Hum. Brain Mapp
PublicationYear 2005
Publisher Wiley Subscription Services, Inc., A Wiley Company
Wiley-Liss
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References Alexander GE, DeLong MR, Strick PL (1986): Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381.
Aron AR, Schlaghecken F, Fletcher PC, Bullmore ET, Eimer M, Barker R, Sahakian BJ, Robbins TW (2003): Inhibition of subliminally primed responses is mediated by the caudate and thalamus: evidence from functional MRI and Huntington's disease. Brain 126: 713-723.
Lebedev MA, Nelson RJ (1999): Rhythmically firing neostriatal neurons in monkey: activity patterns during reaction-time hand movements. J Neurophysiol 82: 1832-1842.
Osman A, Moore CM, Ulrich R (2003): Temporal organization of covert motor processes during response selection and preparation. Biol Psychol 64: 47-75.
Kermadi I, Boussaoud D (1995): Role of the primate striatum in attention and sensorimotor processes: comparison with premotor cortex. Neuroreport 6: 1177-1181.
Mesulam MM (1998): From sensation to cognition. Brain 121: 1013-1052.
Ramsey NF, van den Brink JS, van Muiswinkel AM, Folkers PJ, Moonen CT, Jansma JM, Kahn RS (1998): Phase navigator correction in 3D fMRI improves detection of brain activation: quantitative assessment with a graded motor activation procedure. Neuroimage 8: 240-248.
Fuster JM (1997): The prefrontal cortex: anatomy, physiology, and neuropsychology of the frontal lobe. Philadelphia: Lippincott Williams and Wilkins. 333 p.
Jaeger D, Gilman S, Aldridge JW (1993): Primate basal ganglia activity in a precued reaching task: preparation for movement. Exp Brain Res 95: 51-64.
Apicella P, Scarnati E, Schultz W (1991): Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli. Exp Brain Res 84: 672-675.
Logan GD, Cowan WB (1984): On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91: 295-327.
Dubois B, Defontaines B, Deweer B, Malapani C, Pillon B (1995): Cognitive and behavioral changes in patients with focal lesions of the basal ganglia. Adv Neurol 65: 29-41.
Saint-Cyr JA, Taylor AE, Nicholson K (1995): Behavior and the basal ganglia. Adv Neurol 65: 1-28.
Rolls ET (1994): Neurophysiology and cognitive functions of the striatum. Rev Neurol (Paris) 150: 648-660.
Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994): The basal ganglia and adaptive motor control. Science 265: 1826-1831.
Raemaekers M, Jansma JM, Cahn W, Van der Geest JN, van der Linden JA, Kahn RS, Ramsey NF (2002): Neuronal substrate of the saccadic inhibition deficit in schizophrenia investigated with 3-dimensional event-related functional magnetic resonance imaging. Arch Gen Psychiatry 59: 313-320.
Jueptner M, Weiller C (1998): A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121: 1437-1449.
Blazquez PM, Fujii N, Kojima J, Graybiel AM (2002): A network representation of response probability in the striatum. Neuron 33: 973-982.
Worsley KJ (1994): Local maxima and the expected Euler characteristic of excursion sets of Chi square, F and t fields. Adv Appl Probability 26: 13-42.
Thevenaz P, Ruttimann UE, Unser M (1998): A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7: 27-41.
Augustine JR (1996): Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22: 229-244.
Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE (1997): Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol 77: 1313-1324.
Tanji J (1994): The supplementary motor area in the cerebral cortex. Neurosci Res 19: 251-268.
Band GP, van Boxtel GJ (1999): Inhibitory motor control in stop paradigms: review and reinterpretation of neural mechanisms. Acta Psychol (Amst) 101: 179-211.
Kimura M (1992): Behavioral modulation of sensory responses of primate putamen neurons. Brain Res 578: 204-214.
Mink JW (1996): The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381-425.
Dreher JC, Grafman J (2002): The roles of the cerebellum and basal ganglia in timing and error prediction. Eur J Neurosci 16: 1609-1619.
Nambu A, Kaneda K, Tokuno H, Takada M (2002): Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol 88: 1830-1842.
Kaji R (2001): Basal ganglia as a sensory gating devise for motor control. J Med Invest 48: 142-146.
Owen AM, James M, Leigh PN, Summers BA, Marsden CD, Quinn NP, Lange KW, Robbins TW (1992): Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 115: 1727-1751.
Hauber W (1998): Involvement of basal ganglia transmitter systems in movement initiation. Prog Neurobiol 56: 507-540.
Sardo P, Ravel S, Legallet E, Apicella P (2000): Influence of the predicted time of stimuli eliciting movements on responses of tonically active neurons in the monkey striatum. Eur J Neurosci 12: 1801-1816.
Alexander GE, Crutcher MD (1990): Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266-271.
Friston KJ, Frith CD, Turner R, Frackowiak RS (1995): Characterizing evoked hemodynamics with fMRI. Neuroimage 2: 157-165.
Logan GD, Irwin DE (2000): Don't look! Don't touch! Inhibitory control of eye and hand movements. Psychon Bull Rev 7: 107-112.
Apicella P (2002): Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur J Neurosci 16: 2017-2026.
Logan GD, Schachar RJ, Tannock R (1997): Impulsivity and inhibitory control. Psychol Sci 8: 60-64.
2002; 16
2002; 59
1990; 13
1994; 150
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1999; 82
1995; 6
1997; 8
1994; 265
1984; 91
1993; 95
1997; 77
1994; 19
1986; 9
2000; 12
1991; 84
1995; 65
2002; 88
1992; 115
1992; 578
2003; 126
1998; 7
1998; 121
1998; 56
2003; 64
1996; 22
1998; 8
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References_xml – reference: Alexander GE, DeLong MR, Strick PL (1986): Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381.
– reference: Apicella P (2002): Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur J Neurosci 16: 2017-2026.
– reference: Kermadi I, Boussaoud D (1995): Role of the primate striatum in attention and sensorimotor processes: comparison with premotor cortex. Neuroreport 6: 1177-1181.
– reference: Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE (1997): Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol 77: 1313-1324.
– reference: Mink JW (1996): The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381-425.
– reference: Kaji R (2001): Basal ganglia as a sensory gating devise for motor control. J Med Invest 48: 142-146.
– reference: Kimura M (1992): Behavioral modulation of sensory responses of primate putamen neurons. Brain Res 578: 204-214.
– reference: Worsley KJ (1994): Local maxima and the expected Euler characteristic of excursion sets of Chi square, F and t fields. Adv Appl Probability 26: 13-42.
– reference: Dubois B, Defontaines B, Deweer B, Malapani C, Pillon B (1995): Cognitive and behavioral changes in patients with focal lesions of the basal ganglia. Adv Neurol 65: 29-41.
– reference: Osman A, Moore CM, Ulrich R (2003): Temporal organization of covert motor processes during response selection and preparation. Biol Psychol 64: 47-75.
– reference: Ramsey NF, van den Brink JS, van Muiswinkel AM, Folkers PJ, Moonen CT, Jansma JM, Kahn RS (1998): Phase navigator correction in 3D fMRI improves detection of brain activation: quantitative assessment with a graded motor activation procedure. Neuroimage 8: 240-248.
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– reference: Logan GD, Schachar RJ, Tannock R (1997): Impulsivity and inhibitory control. Psychol Sci 8: 60-64.
– reference: Owen AM, James M, Leigh PN, Summers BA, Marsden CD, Quinn NP, Lange KW, Robbins TW (1992): Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 115: 1727-1751.
– reference: Jaeger D, Gilman S, Aldridge JW (1993): Primate basal ganglia activity in a precued reaching task: preparation for movement. Exp Brain Res 95: 51-64.
– reference: Alexander GE, Crutcher MD (1990): Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266-271.
– reference: Saint-Cyr JA, Taylor AE, Nicholson K (1995): Behavior and the basal ganglia. Adv Neurol 65: 1-28.
– reference: Hauber W (1998): Involvement of basal ganglia transmitter systems in movement initiation. Prog Neurobiol 56: 507-540.
– reference: Sardo P, Ravel S, Legallet E, Apicella P (2000): Influence of the predicted time of stimuli eliciting movements on responses of tonically active neurons in the monkey striatum. Eur J Neurosci 12: 1801-1816.
– reference: Dreher JC, Grafman J (2002): The roles of the cerebellum and basal ganglia in timing and error prediction. Eur J Neurosci 16: 1609-1619.
– reference: Lebedev MA, Nelson RJ (1999): Rhythmically firing neostriatal neurons in monkey: activity patterns during reaction-time hand movements. J Neurophysiol 82: 1832-1842.
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Snippet We used functional magnetic resonance imaging (fMRI) to study the role of the striatum in inhibitory motor control. Subjects had to refrain from responding to...
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StartPage 336
SubjectTerms Adolescent
Adult
basal ganglia
Biological and medical sciences
Brain Mapping
Cerebral Cortex - anatomy & histology
Cerebral Cortex - physiology
Cerebrospinal fluid. Spinal cord. Spinal roots. Spinal nerves
Cognition. Intelligence
Corpus Striatum - anatomy & histology
Corpus Striatum - physiology
Female
fMRI
Functional Laterality - physiology
functional magnetic resonance imaging
Fundamental and applied biological sciences. Psychology
Humans
inhibition
Intellectual and cognitive abilities
Investigative techniques, diagnostic techniques (general aspects)
Magnetic Resonance Imaging
Male
Medical sciences
motor behavior
Movement - physiology
Nervous system
Neural Inhibition - physiology
Neural Pathways - anatomy & histology
Neural Pathways - physiology
Neuropsychological Tests
Neurosurgery
Photic Stimulation
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Psychomotor Performance - physiology
Radiodiagnosis. Nmr imagery. Nmr spectrometry
Reaction Time - physiology
striatum
Surgery (general aspects). Transplantations, organ and tissue grafts. Graft diseases
Volition - physiology
Title Function of striatum beyond inhibition and execution of motor responses
URI https://api.istex.fr/ark:/67375/WNG-5S0WDMP4-J/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhbm.20111
https://www.ncbi.nlm.nih.gov/pubmed/15852388
https://www.proquest.com/docview/17211196
https://www.proquest.com/docview/67949360
https://pubmed.ncbi.nlm.nih.gov/PMC6871687
Volume 25
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