An age-related shift of resting-state functional connectivity of the subthalamic nucleus: A potential mechanism for compensating motor performance decline in older adults

Frontiers in Aging Neuroscience

Volumn 6, Issue JUL, 2014, Pages

  Mathys, Christian ^a   Hoffstaedter, Felix ^a,b   Caspers, Julian ^a,b   Caspers, Svenja ^b   Südmeyer, Martin ^a   Grefkes, Christian ^b,c,d   Eickhoff, Simon B ^a,b   Langner, Robert ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Age related changes; Functional connectivity; Healthy aging; Resting state fMRI; Subthalamic nucleus

Indexed keywords

ADULT; AGING; ANTERIOR CINGULATE; CAUDATE NUCLEUS; CONTROLLED STUDY; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MAJOR CLINICAL STUDY; MOTOR CONTROL; MOTOR PERFORMANCE; PLANT SEED; POSTERIOR CINGULATE; POSTERIOR INSULA; PRECUNEUS; PUTAMEN; REST; SENSORIMOTOR CORTEX; SUBTHALAMIC NUCLEUS; THALAMUS; YOUNG ADULT;

EID: 84987622059     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00178     Document Type: Article

References (101)

1. Alexander, G. E., and Crutcher, M. D. (1990). Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-271. doi: 10.1016/0166-2236(90)90107-L
2. Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., et al. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. 210, 343-352. doi: 10.1007/s00429-005-0025-5
3. Amunts, K., Malikovic, A., Mohlberg, H., Schormann, T., and Zilles, K. (2000). Brodmann's areas 17 and 18 brought into stereotaxic space-where and how variable? Neuroimage 11, 66-84. doi: 10.1006/nimg.1999.0516
4. Amunts, K., Schleicher, A., Burgel, U., Mohlberg, H., Uylings, H. B., and Zilles, K. (1999). Broca's region revisited: cytoarchitecture and intersubject variability. J. Comp. Neurol. 412, 319-341. doi: 10.1002/(SICI)1096-9861(19990920)412:2<319::AID-CNE10>3.0.CO;2-7
5. Amunts, K., Weiss, P. H., Mohlberg, H., Pieperhoff, P., Eickhoff, S., Gurd, J. M., et al. (2004). Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space-the roles of Brodmann areas 44 and 45. Neuroimage 22, 42-56. doi: 10.1016/j.neuroimage.2003.12.031
6. Aravamuthan, B. R., Muthusamy, K. A., Stein, J. F., Aziz, T. Z., and Johansen-Berg, H. (2007). Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage 37, 694-705. doi: 10.1016/j.neuroimage.2007.05.050
7. Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., and Poldrack, R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J. Neurosci. 27, 3743-3752. doi: 10.1523/JNEUROSCI.0519-07.2007
8. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neuroimage 26, 839-851. doi: 10.1016/j.neuroimage.2005.02.018
9. Baudrexel, S., Witte, T., Seifried, C., Von Wegner, F., Beissner, F., Klein, J. C., et al. (2011). Resting state fMRI reveals increased subthalamic nucleus-motor cortex connectivity in Parkinson's disease. Neuroimage 55, 1728-1738. doi: 10.1016/j.neuroimage.2011.01.017
10. Beckmann, M., Johansen-Berg, H., and Rushworth, M. F. (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 29, 1175-1190. doi: 10.1523/JNEUROSCI.3328-08.2009
11. Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., et al. (2003). Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6, 750-757. doi: 10.1038/nn1075
12. Bellebaum, C., Jokisch, D., Gizewski, E. R., Forsting, M., and Daum, I. (2012). The neural coding of expected and unexpected monetary performance outcomes: dissociations between active and observational learning. Behav. Brain Res. 227, 241-251. doi: 10.1016/j.bbr.2011.10.042
13. Biswal, B. B., Mennes, M., Zuo, X. N., Gohel, S., Kelly, C., Smith, S. M., et al. (2010). Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U.S.A. 107, 4734-4739. doi: 10.1073/pnas.0911855107
14. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. doi: 10.1002/mrm.1910340409
15. Brittain, J. S., Watkins, K. E., Joundi, R. A., Ray, N. J., Holland, P., Green, A. L., et al. (2012). A role for the subthalamic nucleus in response inhibition during conflict. J. Neurosci. 32, 13396-13401. doi: 10.1523/JNEUROSCI.2259-12.2012
16. Brown, P., and Marsden, C. D. (1998). What do the basal ganglia do? Lancet 351, 1801-1804. doi: 10.1016/S0140-6736(97)11225-9
17. Brunenberg, E. J., Moeskops, P., Backes, W. H., Pollo, C., Cammoun, L., Vilanova, A., et al. (2012). Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway. PLoS ONE 7:e39061. doi: 10.1371/journal.pone.0039061
18. Caspers, S., Eickhoff, S. B., Geyer, S., Scheperjans, F., Mohlberg, H., Zilles, K., et al. (2008). The human inferior parietal lobule in stereotaxic space. Brain Struct. Funct. 212, 481-495. doi: 10.1007/s00429-008-0195-z
19. Caspers, S., Geyer, S., Schleicher, A., Mohlberg, H., Amunts, K., and Zilles, K. (2006). The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. Neuroimage 33, 430-448. doi: 10.1016/j.neuroimage.2006.06.054
20. Cavanna, A. E., and Trimble, M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564-583. doi: 10.1093/brain/awl004
21. Cieslik, E. C., Zilles, K., Caspers, S., Roski, C., Kellermann, T. S., Jakobs, O., et al. (2013). Is there "one" DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb. Cortex 23, 2677-2689. doi: 10.1093/cercor/bhs256
22. Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences, 2nd Edn. Hillsdale, NJ: LawrenceErlbaum Associates.
23. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59-70. doi: 10.1038/nrn2555
24. de Lau, L. M., and Breteler, M. M. (2006). Epidemiology of Parkinson's disease. Lancet Neurol. 5, 525-535. doi: 10.1016/S1474-4422(06)70471-9
25. Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995). Contributions of anterior cingulate cortex to behaviour. Brain 118, 279-306. doi: 10.1093/brain/118.1.279
26. Diedrichsen, J., Balsters, J. H., Flavell, J., Cussans, E., and Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. Neuroimage 46, 39-46. doi: 10.1016/j.neuroimage.2009.01.045
27. Eckert, U., Metzger, C. D., Buchmann, J. E., Kaufmann, J., Osoba, A., Li, M., et al. (2012). Preferential networks of the mediodorsal nucleus and centromedian-parafascicular complex of the thalamus-a DTI tractography study. Hum. Brain Mapp. 33, 2627-2637. doi: 10.1002/hbm.21389
28. Eickhoff, S. B., Amunts, K., Mohlberg, H., and Zilles, K. (2006a). The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. Cereb. Cortex 16, 268-279. doi: 10.1093/cercor/bhi106
29. Eickhoff, S. B., Schleicher, A., Zilles, K., and Amunts, K. (2006b). The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb. Cortex 16, 254-267. doi: 10.1093/cercor/bhi105
30. Eickhoff, S. B., Paus, T., Caspers, S., Grosbras, M. H., Evans, A. C., Zilles, K., et al. (2007). Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36, 511-521. doi: 10.1016/j.neuroimage.2007.03.060
31. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. doi: 10.1038/nrn2201
32. Frank, M. J. (2006). Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw. 19, 1120-1136. doi: 10.1016/j.neunet.2006.03.006
33. Frank, M. J., Samanta, J., Moustafa, A. A., and Sherman, S. J. (2007). Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 318, 1309-1312. doi: 10.1126/science.1146157
34. Geyer, S. (2004). The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Adv. Anat. Embryol. Cell Biol. 174, I-VIII, 1-89. doi: 10.1007/978-3-642-18910-4_1
35. Geyer, S., Ledberg, A., Schleicher, A., Kinomura, S., Schormann, T., Burgel, U., et al. (1996). Two different areas within the primary motor cortex of man. Nature 382, 805-807. doi: 10.1038/382805a0
36. Geyer, S., Schleicher, A., and Zilles, K. (1999). Areas 3a, 3b, and 1 of human primary somatosensory cortex. Neuroimage 10, 63-83. doi: 10.1006/nimg.1999.0440
37. Geyer, S., Schormann, T., Mohlberg, H., and Zilles, K. (2000). Areas 3a, 3b, and 1 of human primary somatosensory cortex. Part 2. Spatial normalization to standard anatomical space. Neuroimage 11, 684-696. doi: 10.1006/nimg.2000.0548
38. Goble, D. J., Coxon, J. P., Van Impe, A., Geurts, M., Van Hecke, W., Sunaert, S., et al. (2012). The neural basis of central proprioceptive processing in older versus younger adults: an important sensory role for right putamen. Hum. Brain Mapp. 33, 895-908. doi: 10.1002/hbm.21257
39. Gouix, E., Buisson, A., Nieoullon, A., Kerkerian-Le Goff, L., Tauskela, J. S., Blondeau, N., et al. (2014). Oxygen glucose deprivation-induced astrocyte dysfunction provokes neuronal death through oxidative stress. Pharmacol. Res. 11, 8-17. doi: 10.1016/j.phrs.2014.06.002
40. Grady, C. L. (2005). "Functional connectivity during memory tasks in healthy aging and dementia, " in Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging, eds R. Cabeza, L. Nyberg, and D. C. Park (Oxford: Oxford University Press), 286-308.
41. Grahn, J. A., Parkinson, J. A., and Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Prog. Neurobiol. 86, 141-155. doi: 10.1016/j.pneurobio.2008.09.004
42. Graybiel, A. M. (2005). The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 15, 638-644. doi: 10.1016/j.conb.2005.10.006
43. Grefkes, C., Geyer, S., Schormann, T., Roland, P., and Zilles, K. (2001). Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. Neuroimage 14, 617-631. doi: 10.1006/nimg.2001.0858
44. Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A 100, 253-258. doi: 10.1073/pnas.0135058100
45. Hamani, C., Saint-Cyr, J. A., Fraser, J., Kaplitt, M., and Lozano, A. M. (2004). The subthalamic nucleus in the context of movement disorders. Brain 127, 4-20. doi: 10.1093/brain/awh029
46. Harada, T., Miyai, I., Suzuki, M., and Kubota, K. (2009). Gait capacity affects cortical activation patterns related to speed control in the elderly. Exp. Brain Res. 193, 445-454. doi: 10.1007/s00221-008-1643-y
47. Hardwick, R. M., Rottschy, C., Miall, R. C., and Eickhoff, S. B. (2013). A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67, 283-297. doi: 10.1016/j.neuroimage.2012.11.020
48. Heuninckx, S., Wenderoth, N., Debaere, F., Peeters, R., and Swinnen, S. P. (2005). Neural basis of aging: the penetration of cognition into action control. J. Neurosci. 25, 6787-6796. doi: 10.1523/JNEUROSCI.1263-05.2005
49. Hoffstaedter, F., Grefkes, C., Caspers, S., Roski, C., Palomero-Gallagher, N., Laird, A. R., et al. (2013a). The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum. Brain Mapp. 35, 2741-2753. doi: 10.1002/hbm.22363
50. Hoffstaedter, F., Grefkes, C., Zilles, K., and Eickhoff, S. B. (2013b). The "what" and "when" of self-initiated movements. Cereb. Cortex 23, 520-530. doi: 10.1093/cercor/bhr391
51. Hoffstaedter, F., Grefkes, C., Roski, C., Caspers, S., Zilles, K., and Eickhoff, S. B. (2014). Age-related decrease of functional connectivity additional to gray matter atrophy in a network for movement initiation. Brain Struct. Funct. doi: 10.1007/s00429-013-0696-2 [Epub ahead of print].
52. Jakobs, O., Langner, R., Caspers, S., Roski, C., Cieslik, E. C., Zilles, K., et al. (2012). Across-study and within-subject functional connectivity of a right temporo-parietal junction subregion involved in stimulus-context integration. Neuroimage 60, 2389-2398. doi: 10.1016/j.neuroimage.2012.02.037
53. Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S., and Passingham, R. E. (1997). Anatomy of motor learning. I. Frontal cortex and attention to action. J. Neurophysiol. 77, 1313-1324.
54. Kelly, A. M., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., et al. (2009). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cereb. Cortex 19, 640-657. doi: 10.1093/cercor/bhn117
55. Kelly, C., Toro, R., Di Martino, A., Cox, C. L., Bellec, P., Castellanos, F. X., et al. (2012). A convergent functional architecture of the insula emerges across imaging modalities. Neuroimage 61, 1129-1142. doi: 10.1016/j.neuroimage.2012.03.021
56. Keuken, M. C., Bazin, P. L., Schafer, A., Neumann, J., Turner, R., and Forstmann, B. U. (2013). Ultra-high 7T MRI of structural age-related changes of the subthalamic nucleus. J. Neurosci. 33, 4896-4900. doi: 10.1523/JNEUROSCI.3241-12.2013
57. Kraft, E., Chen, A. W., Flaherty, A. W., Blood, A. J., Kwong, K. K., and Jenkins, B. G. (2007). The role of the basal ganglia in bimanual coordination. Brain Res. 1151, 62-73. doi: 10.1016/j.brainres.2007.01.142
58. Kuhn, A. A., Tsui, A., Aziz, T., Ray, N., Brucke, C., Kupsch, A., et al. (2009). Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp. Neurol. 215, 380-387. doi: 10.1016/j.expneurol.2008.11.008
59. Kurth, F., Eickhoff, S. B., Schleicher, A., Hoemke, L., Zilles, K., and Amunts, K. (2010a). Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cereb. Cortex 20, 1448-1461. doi: 10.1093/cercor/bhp208
60. Kurth, F., Zilles, K., Fox, P. T., Laird, A. R., and Eickhoff, S. B. (2010b). A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 214, 519-534. doi: 10.1007/s00429-010-0255-z
61. Lambert, C., Zrinzo, L., Nagy, Z., Lutti, A., Hariz, M., Foltynie, T., et al. (2012). Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage 60, 83-94. doi: 10.1016/j.neuroimage.2011.11.082
62. Langner, R., Cieslik, E. C., Behrwind, S. D., Roski, C., Caspers, S., Amunts, K., et al. (2014). Aging and response conflict solution: behavioural and functional connectivity changes. Brain Struct. Funct. doi: 10.1007/s00429-014-0758-0 [Epub ahead of print].
63. Langner, R., Kellermann, T., Boers, F., Sturm, W., Willmes, K., and Eickhoff, S. B. (2011). Modality-specific perceptual expectations selectively modulate baseline activity in auditory, somatosensory, and visual cortices. Cereb. Cortex 21, 2850-2862. doi: 10.1093/cercor/bhr083
64. Langner, R., Kellermann, T., Eickhoff, S. B., Boers, F., Chatterjee, A., Willmes, K., et al. (2012). Staying responsive to the world: modality-specific and-nonspecific contributions to speeded auditory, tactile, and visual stimulus detection. Hum. Brain Mapp. 33, 398-418. doi: 10.1002/hbm.21220
65. Lee, T. M., Zhang, J. X., Chan, C. C., Yuen, K. S., Chu, L. W., Cheung, R. T., et al. (2006). Age-related differences in response regulation as revealed by functional MRI. Brain Res. 1076, 171-176. doi: 10.1016/j.brainres.2005.12.124
66. Leech, R., and Sharp, D. J. (2013). The role of the posterior cingulate cortex in cognition and disease. Brain 137, 12-32. doi: 10.1093/brain/awt162
67. Le Jeune, F., Peron, J., Grandjean, D., Drapier, S., Haegelen, C., Garin, E., et al. (2010). Subthalamic nucleus stimulation affects limbic and associative circuits: a PET study. Eur. J. Nucl. Med. Mol. Imaging 37, 1512-1520. doi: 10.1007/s00259-010-1436-y
68. Limousin, P., Pollak, P., Benazzouz, A., Hoffmann, D., Le Bas, J. F., Broussolle, E., et al. (1995). Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345, 91-95. doi: 10.1016/S0140-6736(95)90062-4
69. Madden, D. J., Costello, M. C., Dennis, N. A., Davis, S. W., Shepler, A. M., Spaniol, J., et al. (2010). Adult age differences in functional connectivity during executive control. Neuroimage 52, 643-657. doi: 10.1016/j.neuroimage.2010.04.249
70. Manes, J. L., Parkinson, A. L., Larson, C. R., Greenlee, J. D., Eickhoff, S. B., Corcos, D. M., et al. (2013). Connectivity of the subthalamic nucleus and globus pallidus pars interna to regions within the speech network: a meta-analytic connectivity study. Hum. Brain Mapp. 35. doi: 10.1002/hbm.22417
71. Mansfield, E. L., Karayanidis, F., Jamadar, S., Heathcote, A., and Forstmann, B. U. (2011). Adjustments of response threshold during task switching: a model-based functional magnetic resonance imaging study. J. Neurosci. 31, 14688-14692. doi: 10.1523/JNEUROSCI.2390-11.2011
72. Margulies, D. S., Kelly, A. M., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., and Milham, M. P. (2007). Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37, 579-588. doi: 10.1016/j.neuroimage.2007.05.019
73. Meier, J. D., Aflalo, T. N., Kastner, S., and Graziano, M. S. (2008). Complex organization of human primary motor cortex: a high-resolution fMRI study. J. Neurophysiol. 100, 1800-1812. doi: 10.1152/jn.90531.2008
74. Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C. E., Benazzouz, A., et al. (2005). Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128, 2372-2382. doi: 10.1093/brain/awh616
75. Mitchell, K. J., Raye, C. L., Ebner, N. C., Tubridy, S. M., Frankel, H., and Johnson, M. K. (2009). Age-group differences in medial cortex activity associated with thinking about self-relevant agendas. Psychol. Aging 24, 438-449. doi: 10.1037/a0015181
76. Nambu, A., Tokuno, H., and Takada, M. (2002). Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci. Res. 43, 111-117. doi: 10.1016/S0168-0102(02)00027-5
77. Noble, J. W., Eng, J. J., Kokotilo, K. J., and Boyd, L. A. (2011). Aging effects on the control of grip force magnitude: an fMRI study. Exp. Gerontol. 46, 453-461. doi: 10.1016/j.exger.2011.01.004
78. Northoff, G., Heinzel, A., De Greck, M., Bermpohl, F., Dobrowolny, H., and Panksepp, J. (2006). Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage 31, 440-457. doi: 10.1016/j.neuroimage.2005.12.002
79. Packard, M. G., and Knowlton, B. J. (2002). Learning and memory functions of the Basal Ganglia. Annu. Rev. Neurosci. 25, 563-593. doi: 10.1146/annurev.neuro.25112701.142937
80. Pollok, B., Kamp, D., Butz, M., Wojtecki, L., Timmermann, L., Sudmeyer, M., et al. (2013). Increased SMA-M1 coherence in Parkinson's disease-pathophysiology or compensation? Exp. Neurol. 247, 178-181. doi: 10.1016/j.expneurol.2013.04.013
81. Popa-Wagner, A., Buga, A. M., Popescu, B., and Muresanu, D. (2013). Vascular cognitive impairment, dementia, aging and energy demand. A vicious cycle. J. Neural Transm. doi: 10.1007/s00702-013-1129-3 [Epub ahead of print].
82. Qin, P., and Northoff, G. (2011). How is our self related to midline regions and the default-mode network? Neuroimage 57, 1221-1233. doi: 10.1016/j.neuroimage.2011.05.028
83. Rorden, C., and Brett, M. (2000). Stereotaxic display of brain lesions. Behav. Neurol. 12, 191-200. doi: 10.1155/2000/421719
84. Rottschy, C., Eickhoff, S. B., Schleicher, A., Mohlberg, H., Kujovic, M., Zilles, K., et al. (2007). Ventral visual cortex in humans: cytoarchitectonic mapping of two extrastriate areas. Hum. Brain Mapp. 28, 1045-1059. doi: 10.1002/hbm.20348
85. Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Williams, S. C., Simmons, A., et al. (1999). Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am. J. Psychiatry 156, 891-896. doi: 10.1176/appi.pn.2014.2a3
86. Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., et al. (2013a). An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64, 240-256. doi: 10.1016/j.neuroimage.2012.08.052
87. Satterthwaite, T. D., Wolf, D. H., Ruparel, K., Erus, G., Elliott, M. A., Eickhoff, S. B., et al. (2013b). Heterogeneous impact of motion on fundamental patterns of developmental changes in functional connectivity during youth. Neuroimage 83, 45-57. doi: 10.1016/j.neuroimage.2013.06.045
88. Schafer, A., Forstmann, B. U., Neumann, J., Wharton, S., Mietke, A., Bowtell, R., et al. (2012). Direct visualization of the subthalamic nucleus and its iron distribution using high-resolution susceptibility mapping. Hum. Brain Mapp. 33, 2831-2842. doi: 10.1002/hbm.21404
89. Scheperjans, F., Eickhoff, S. B., Homke, L., Mohlberg, H., Hermann, K., Amunts, K., et al. (2008a). Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. Cereb. Cortex 18, 2141-2157. doi: 10.1093/cercor/bhm241
90. Scheperjans, F., Hermann, K., Eickhoff, S. B., Amunts, K., Schleicher, A., and Zilles, K. (2008b). Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. Cereb. Cortex 18, 846-867. doi: 10.1093/cercor/bhm116
91. Schilbach, L., Bzdok, D., Timmermans, B., Fox, P. T., Laird, A. R., Vogeley, K., et al. (2012). Introspective minds: using ALE meta-analyses to study commonalities in the neural correlates of emotional processing, social & unconstrained cognition. PLoS ONE 7:e30920. doi: 10.1371/journal.pone.0030920
92. Scholz, V. H., Flaherty, A. W., Kraft, E., Keltner, J. R., Kwong, K. K., Chen, Y. I., et al. (2000). Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks. Brain Res. 879, 204-215. doi: 10.1016/S0006-8993(00)02749-9
93. Seidler, R. D. (2006). Differential effects of age on sequence learning and sensorimotor adaptation. Brain Res. Bull. 70, 337-346. doi: 10.1016/j.brainresbull.2006.06.008
94. Seidler, R. D., Bernard, J. A., Burutolu, T. B., Fling, B. W., Gordon, M. T., Gwin, J. T., et al. (2010). Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 34, 721-733. doi: 10.1016/j.neubiorev.2009.10.005
95. Szewczyk-Krolikowski, K., Tomlinson, P., Nithi, K., Wade-Martins, R., Talbot, K., Ben-Shlomo, Y., et al. (2014). The influence of age and gender on motor and non-motor features of early Parkinson's disease: initial findings from the Oxford Parkinson Disease Center (OPDC) discovery cohort. Parkinsonism relat. disord. 20, 99-105. doi: 10.1016/j.parkreldis.2013.09.025
96. Temel, Y., Blokland, A., Steinbusch, H. W., and Visser-Vandewalle, V. (2005). The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog. Neurobiol. 76, 393-413. doi: 10.1016/j.pneurobio.2005.09.005
97. Tommasi, G., Krack, P., Fraix, V., and Pollak, P. (2012). Effects of varying subthalamic nucleus stimulation on apraxia of lid opening in Parkinson's disease. J. Neurol. 259, 1944-1950. doi: 10.1007/s00415-012-6447-0
98. Ward, N. S., Swayne, O. B., and Newton, J. M. (2008). Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol. Aging 29, 1434-1446. doi: 10.1016/j.neurobiolaging.2007.04.017
99. Weintraub, D. B., and Zaghloul, K. A. (2013). The role of the subthalamic nucleus in cognition. Rev. Neurosci. 24, 125-138. doi: 10.1515/revneuro-2012-0075
100. Williams, Z. M., and Eskandar, E. N. (2006). Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat. Neurosci. 9, 562-568. doi: 10.1038/nn1662
101. Zilles, K., and Amunts, K. (2010). Centenary of Brodmann's map-conception and fate. Nature reviews. Neuroscience 11, 139-145. doi: 10.1038/nrn2776