Motivational tuning of fronto-subthalamic connectivity facilitates control of action impulses

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3210-3217

  Herz, Damian M ^a   Christensen, Mark S ^a,b   Bruggemann, Norbert ^a   Hulme, Oliver J ^a   Richard Ridderinkhof, K ^c   Madsen, Kristoffer H ^a,d   Siebner, Hartwig R ^a,b,e  

^a HVIDOVRE HOSPITAL   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e BISPEBJERG HOSPITAL   (Denmark)

Author keywords

fMRI; Motor control; Pre SMA; Reward; Simon task; TMS

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CAUSAL MODELING; CONNECTOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMPULSIVENESS; INFERIOR FRONTAL GYRUS; MALE; MOTIVATION; MOTOR CONTROL; NERVE CONDUCTION; NORMAL HUMAN; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS; SUPPLEMENTARY MOTOR AREA; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL STIMULATION;

FMRI; MOTOR CONTROL; PRE-SMA; REWARD; SIMON TASK; TMS;

ADULT; CHOICE BEHAVIOR; CUES; FEMALE; FRONTAL LOBE; HEALTHY VOLUNTEERS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MOTIVATION; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SUBTHALAMUS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84894429297     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4081-13.2014     Document Type: Article

References (54)

1. Aarts E, van Holstein M, Cools R (2011) Striatal dopamine and the interface between motivation and cognition. Front Psychol 2:163. CrossRef Medline
2. Aarts E, Helmich RC, Janssen MJ, Oyen WJ, Bloem BR, Cools R (2012) Aberrant reward processing in Parkinson's disease is associated with dopamine cell loss. Neuroimage 59:3339-3346. CrossRef Medline
3. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381. CrossRef Medline
4. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69:e55-68. CrossRef Medline
5. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007) Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27:3743-3752. CrossRef Medline
6. Ballanger B, van Eimeren T, Moro E, Lozano AM, Hamani C, Boulinguez P, Pellecchia G, Houle S, Poon YY, Lang AE, Strafella AP (2009) Stimulation of the subthalamic nucleus and impulsivity: release your horses. Ann Neurol 66:817-824. CrossRef Medline
7. Belin D, Everitt BJ (2008) Cocaine seeking habits depend upon dopaminedependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57:432-441. CrossRef Medline
8. Calabresi P, Picconi B, Tozzi A, Di Filippo M (2007) Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci 30:211-219. CrossRef Medline
9. Cavanagh JF, Wiecki TV, Cohen MX, Figueroa CM, Samanta J, Sherman SJ, Frank MJ (2011) Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci 14:1462-1467. CrossRef Medline
10. Forstmann BU, van den Wildenberg WP, Ridderinkhof KR (2008) Neural mechanisms, temporal dynamics, and individual differences in interference control. J Cogn Neurosci 20:1854-1865. CrossRef Medline
11. Forstmann BU, Anwander A, Schäfer A, Neumann J, Brown S, Wagenmakers EJ, Bogacz R, Turner R (2010) Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci U S A 107:15916-15920. CrossRef Medline
12. Frank MJ, Seeberger LC, O'Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306:1940-1943. CrossRef Medline
13. Frank MJ, Samanta J, Moustafa AA, Sherman SJ (2007) Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 318:1309-1312. CrossRef Medline
14. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346-355. CrossRef Medline
15. Friston KJ, Harrison L, PennyW (2003) Dynamic causal modelling. Neuroimage 19:1273-1302. CrossRef Medline
16. Friston K, Mattout J, Trujillo-Barreto N, Ashburner J, Penny W (2007) Variational free energy and the Laplace approximation. Neuroimage 34: 220-234. CrossRef Medline
17. Haber SN, Kim KS, Mailly P, Calzavara R (2006) Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26:8368-8376. CrossRef Medline
18. Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC (2013) The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 23:1593-1605. CrossRef Medline
19. Harsay HA, Cohen MX, Oosterhof NN, Forstmann BU, Mars RB, Ridderinkhof KR (2011) Functional connectivity of the striatum links motivation to action control in humans. J Neurosci 31:10701-10711. CrossRef Medline
20. Hikosaka O, IsodaM (2010) Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms. Trends Cogn Sci 14:154-161. CrossRef Medline
21. Hirose S, Chikazoe J, Watanabe T, Jimura K, Kunimatsu A, Abe O, Ohtomo K, Miyashita Y, Konishi S (2012) Efficiency of go/no-go task performance implemented in the left hemisphere. J Neurosci 32:9059-9065. CrossRef Medline
22. Hommel B, Proctor RW, Vu KP (2004) A feature-integration account of sequential effects in the Simon task. Psychol Res 68:1-17. CrossRef Medline
23. Jahfari S, Verbruggen F, Frank MJ, Waldorp LJ, Colzato L, Ridderinkhof KR, Forstmann BU (2012) How preparation changes the need for top-down control of the basal ganglia when inhibiting premature actions. J Neurosci 32:10870-10878. CrossRef Medline
24. Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci U S A 101:13335-13340. CrossRef Medline
25. Kornblum S, Hasbroucq T, Osman A (1990) Dimensional overlap: cognitive basis for stimulus-response compatibility-a model and taxonomy. Psychol Rev 97:253-270. CrossRef Medline
26. Kosslyn SM, Cacioppo JT, Davidson RJ, Hugdahl K, Lovallo WR, Spiegel D, Rose R (2002) Bridging psychology and biology. The analysis of individuals in groups. Am Psychol 57:341-351. CrossRef Medline
27. Lambert C, Zrinzo L, Nagy Z, Lutti A, Hariz M, Foltynie T, Draganski B, Ashburner J, Frackowiak R (2012) Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and subparcellation using diffusion weighted imaging. Neuroimage 60:83-94. CrossRef Medline
28. Lucerna S, Salpietro FM, Alafaci C, Tomasello F (2002) In vivo atlas of deep brain structures, Vol 1. Berlin: Springer.
29. Lund TE, Madsen KH, Sidaros K, Luo WL, Nichols TE (2006) Non-white noise in fMRI: does modelling have an impact? Neuroimage 29:54-66. CrossRef Medline
30. Magill PJ, Sharott A, Bevan MD, Brown P, Bolam JP (2004) Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J Neurophysiol 92:700-714. CrossRef Medline
31. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97. CrossRef Medline
32. Monakow KH, Akert K, Künzle H (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp Brain Res 33:395-403. Medline
33. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43:111-117. CrossRef Medline
34. Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MF (2010) Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc Natl Acad Sci U S A 107:13240-13245. CrossRef Medline
35. Obeso I, Cho SS, Antonelli F, Houle S, Jahanshahi M, Ko JH, Strafella AP (2013) Stimulation of the pre-SMA influences cerebral blood flow in frontal areas involved with inhibitory control of action. Brain Stimul 6:769-776. CrossRef Medline
36. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113. CrossRef Medline
37. Penny WD, Stephan KE, Mechelli A, Friston KJ (2004) Comparing dynamic causal models. Neuroimage 22:1157-1172. CrossRef Medline
38. Peterson TC, Villatoro L, Arneson T, Ahuja B, Voss S, Swain RA (2012) Behavior modification after inactivation of cerebellar dentate nuclei. Behav Neurosci 126:551-562. CrossRef Medline
39. Prescott IA, Dostrovsky JO, Moro E, Hodaie M, Lozano AM, HutchisonWD (2009) Levodopa enhances synaptic plasticity in the substantia nigra pars reticulata of Parkinson's disease patients. Brain 132:309-318. CrossRef Medline
40. Ramnani N (2006) The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7:511-522. CrossRef Medline
41. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, Agid Y, DeLong MR, Obeso JA (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat Rev Neurosci 11:760-772. CrossRef Medline
42. Ridderinkhof KR (2002) Micro-and macro-adjustments of task set: activation and suppression in conflict tasks. Psychol Res 66:312-323. CrossRef Medline
43. Ridderinkhof KR, Forstmann BU, Wylie SA, Burle B, van den Wildenberg WPM (2011) Neurocognitive mechanisms of action control: resisting the call of the Sirens. WIREs Cogn Sci 2:174-192. CrossRef
44. Robbins TW, Everitt BJ (2007) A role for mesencephalic dopamine in activation: commentary on Berridge (2006). Psychopharmacology 191:433-437. CrossRef Medline
45. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, Simmons A, Williams SC, Giampietro V, Andrew CM, Taylor E (2001) Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13:250-261. CrossRef Medline
46. Rushworth MF, Hadland KA, Paus T, Sipila PK (2002) Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. J Neurophysiol 87:2577-2592. Medline
47. Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1-16. CrossRef Medline
48. Simon JR (1967) Ear preference in a simple reaction-time task. J Exp Psychol 75:49-55. CrossRef Medline
49. Soutschek A, Taylor PC, Müller HJ, Schubert T (2013) Dissociable networks control conflict during perception and response selection: a transcranial magnetic stimulation Study. J Neurosci 33:5647-5654. CrossRef Medline
50. Swann NC, Cai W, Conner CR, Pieters TA, Claffey MP, George JS, Aron AR, Tandon N (2012) Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: electrophysiological responses and functional and structural connectivity. Neuroimage 59: 2860-2870. CrossRef Medline
51. Swann N, Poizner H, Houser M, Gould S, Greenhouse I, Cai W, Strunk J, George J, Aron AR (2011) Deep brain stimulation of the subthalamic nucleus alters the cortical profile of response inhibition in the beta frequency band: a scalp EEG study in Parkinson's disease. J Neurosci 31: 5721-5729. CrossRef Medline
52. van den Wildenberg WP, van Boxtel GJ, van der Molen MW, Bosch DA, Speelman JD, Brunia CH (2006) Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson's disease. J Cogn Neurosci 18:626-636. CrossRef Medline
53. Wiecki TV, Frank MJ (2010) Neurocomputational models of motor and cognitive deficits in Parkinson's disease. Prog Brain Res 183:275-297. CrossRef Medline
54. Wylie SA, Ridderinkhof KR, Elias WJ, Frysinger RC, Bashore TR, Downs KE, van Wouwe NC, van den Wildenberg WP (2010) Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson's disease. Brain 133:3611-3624. CrossRef Medline