 |
The Journal of Neuroscience, March 1, 2006, 26(9):2424-2433; doi:10.1523/JNEUROSCI.4682-05.2006
Previous Article | Next Article 
Behavioral/Systems/Cognitive
Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus
Adam R. Aron and
Russell A. Poldrack
Department of Psychology and Brain Research Institute, University of California, Los Angeles, California 90095
Correspondence should be addressed to Dr. Adam R. Aron, Department of Psychology, Franz Hall, Box 951563, University of California, Los Angeles, CA 90095. Email: adamaron{at}ucla.edu
Suppressing an already initiated manual response depends critically on the right inferior frontal cortex (IFC), yet it is unclear how this inhibitory function is implemented in the motor system. It has been suggested that the subthalamic nucleus (STN), which is a part of the basal ganglia, may play a role because it is well placed to suppress the "direct" fronto-striatal pathway that is activated by response initiation. In two experiments, we investigated this hypothesis with functional magnetic resonance imaging and a Stop-signal task. Subjects responded to Go signals and attempted to inhibit the initiated response to occasional Stop signals. In experiment 1, Going significantly activated frontal, striatal, pallidal, and motor cortical regions, consistent with the direct pathway, whereas Stopping significantly activated right IFC and STN. In addition, Stopping-related activation was significantly greater for fast inhibitors than slow ones in both IFC and STN, and activity in these regions was correlated across subjects. In experiment 2, high-resolution functional and structural imaging confirmed the location of Stopping activation within the vicinity of the STN. We propose that the role of the STN is to suppress thalamocortical output, thereby blocking Go response execution. These results provide convergent data for a role for the STN in Stop-signal response inhibition. They also suggest that the speed of Go and Stop processes could relate to the relative activation of different neural pathways. Future research is required to establish whether Stop-signal inhibition could be implemented via a direct functional neuroanatomic projection between IFC and STN (a "hyperdirect" pathway).
Key words: striatum; frontal; activation; fMRI; cognitive control; imaging; Parkinsons disease
Received Nov. 1, 2005;
revised Jan. 11, 2006;
accepted Jan. 19, 2006.
Correspondence should be addressed to Dr. Adam R. Aron, Department of Psychology, Franz Hall, Box 951563, University of California, Los Angeles, CA 90095. Email: adamaron{at}ucla.edu
This article has been cited by other articles:

|
 |

|
 |
 
P. S. Lee, B. E. Yerys, A. Della Rosa, J. Foss-Feig, K. A. Barnes, J. D. James, J. VanMeter, C. J. Vaidya, W. D. Gaillard, and L. E. Kenworthy
Functional Connectivity of the Inferior Frontal Cortex Changes with Age in Children with Autism Spectrum Disorders: A fcMRI Study of Response Inhibition
Cereb Cortex,
August 1, 2009;
19(8):
1787 - 1794.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. T. S. Pattinson, R. J. Governo, B. J. MacIntosh, E. C. Russell, D. R. Corfield, I. Tracey, and R. G. Wise
Opioids Depress Cortical Centers Responsible for the Volitional Control of Respiration
J. Neurosci.,
June 24, 2009;
29(25):
8177 - 8186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Stevenson, J. K. Elsley, and B. D. Corneil
A "Gap Effect" on Stop Signal Reaction Times in a Human Saccadic Countermanding Task
J Neurophysiol,
February 1, 2009;
101(2):
580 - 590.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. M. McAlonan, V. Cheung, S. E. Chua, J. Oosterlaan, S.-f. Hung, C.-p. Tang, C.-c. Lee, S.-l. Kwong, T.-p. Ho, C. Cheung, et al.
Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder
The British Journal of Psychiatry,
February 1, 2009;
194(2):
123 - 129.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. N. Boehler, T. F. Munte, R. M. Krebs, H. -J. Heinze, M. A. Schoenfeld, and J. -M. Hopf
Sensory MEG Responses Predict Successful and Failed Inhibition in a Stop-Signal Task
Cereb Cortex,
January 1, 2009;
19(1):
134 - 145.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Chikazoe, K. Jimura, T. Asari, K.-i. Yamashita, H. Morimoto, S. Hirose, Y. Miyashita, and S. Konishi
Functional Dissociation in Right Inferior Frontal Cortex during Performance of Go/No-Go Task
Cereb Cortex,
January 1, 2009;
19(1):
146 - 152.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Barch, T. S. Braver, C. S. Carter, R. A. Poldrack, and T. W. Robbins
CNTRICS Final Task Selection: Executive Control
Schizophr Bull,
January 1, 2009;
35(1):
115 - 135.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Xue, D. G. Ghahremani, and R. A. Poldrack
Neural Substrates for Reversing Stimulus-Outcome and Stimulus-Response Associations
J. Neurosci.,
October 29, 2008;
28(44):
11196 - 11204.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. U. Forstmann, S. Jahfari, H. S. Scholte, U. Wolfensteller, W. P. M. van den Wildenberg, and K. R. Ridderinkhof
Function and Structure of the Right Inferior Frontal Cortex Predict Individual Differences in Response Inhibition: A Model-Based Approach
J. Neurosci.,
September 24, 2008;
28(39):
9790 - 9796.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Xue, A. R. Aron, and R. A. Poldrack
Common Neural Substrates for Inhibition of Spoken and Manual Responses
Cereb Cortex,
August 1, 2008;
18(8):
1923 - 1932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Isoda and O. Hikosaka
Role for Subthalamic Nucleus Neurons in Switching from Automatic to Controlled Eye Movement
J. Neurosci.,
July 9, 2008;
28(28):
7209 - 7218.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. R. Wylie, J. J. Foxe, and T. L. Taylor
Forgetting as an Active Process: An fMRI Investigation of Item-Method-Directed Forgetting
Cereb Cortex,
March 1, 2008;
18(3):
670 - 682.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. E. Emeric, J. W. Brown, M. Leslie, P. Pouget, V. Stuphorn, and J. D. Schall
Performance Monitoring Local Field Potentials in the Medial Frontal Cortex of Primates: Anterior Cingulate Cortex
J Neurophysiol,
February 1, 2008;
99(2):
759 - 772.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Eagle, C. Baunez, D. M. Hutcheson, O. Lehmann, A. P. Shah, and T. W. Robbins
Stop-Signal Reaction-Time Task Performance: Role of Prefrontal Cortex and Subthalamic Nucleus
Cereb Cortex,
January 1, 2008;
18(1):
178 - 188.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Baym, B. A. Corbett, S. B. Wright, and S. A. Bunge
Neural correlates of tic severity and cognitive control in children with Tourette syndrome
Brain,
January 1, 2008;
131(1):
165 - 179.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. D. Chambers, M. A. Bellgrove, I. C. Gould, T. English, H. Garavan, E. McNaught, M. Kamke, and J. B. Mattingley
Dissociable Mechanisms of Cognitive Control in Prefrontal and Premotor Cortex
J Neurophysiol,
December 1, 2007;
98(6):
3638 - 3647.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Aron, S. Durston, D. M. Eagle, G. D. Logan, C. M. Stinear, and V. Stuphorn
Converging Evidence for a Fronto-Basal-Ganglia Network for Inhibitory Control of Action and Cognition
J. Neurosci.,
October 31, 2007;
27(44):
11860 - 11864.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. C. J. Taylor, A. C. Nobre, and M. F. S. Rushworth
Subsecond Changes in Top Down Control Exerted by Human Medial Frontal Cortex during Conflict and Action Selection: A Combined Transcranial Magnetic Stimulation Electroencephalography Study
J. Neurosci.,
October 17, 2007;
27(42):
11343 - 11353.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J Frank, A. Scheres, and S. J Sherman
Understanding decision-making deficits in neurological conditions: insights from models of natural action selection
Phil Trans R Soc B,
September 29, 2007;
362(1485):
1641 - 1654.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Tomassini, S. Jbabdi, J. C. Klein, T. E. J. Behrens, C. Pozzilli, P. M. Matthews, M. F. S. Rushworth, and H. Johansen-Berg
Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations
J. Neurosci.,
September 19, 2007;
27(38):
10259 - 10269.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-C. Leung and W. Cai
Common and Differential Ventrolateral Prefrontal Activity during Inhibition of Hand and Eye Movements
J. Neurosci.,
September 12, 2007;
27(37):
9893 - 9900.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Brefczynski-Lewis, A. Lutz, H. S. Schaefer, D. B. Levinson, and R. J. Davidson
Neural correlates of attentional expertise in long-term meditation practitioners
PNAS,
July 3, 2007;
104(27):
11483 - 11488.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Aron
The Neural Basis of Inhibition in Cognitive Control
Neuroscientist,
June 1, 2007;
13(3):
214 - 228.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
T.W Robbins
Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications
Phil Trans R Soc B,
May 29, 2007;
362(1481):
917 - 932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Aron, T. E. Behrens, S. Smith, M. J. Frank, and R. A. Poldrack
Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI
J. Neurosci.,
April 4, 2007;
27(14):
3743 - 3752.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P. Coxon, C. M. Stinear, and W. D. Byblow
Selective Inhibition of Movement
J Neurophysiol,
March 1, 2007;
97(3):
2480 - 2489.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P. Coxon, C. M. Stinear, and W. D. Byblow
Intracortical Inhibition During Volitional Inhibition of Prepared Action
J Neurophysiol,
June 1, 2006;
95(6):
3371 - 3383.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|