Individual Differences in Premotor Brain Systems Underlie Behavioral Apathy

Cerebral Cortex

Volumn 26, Issue 2, 2016, Pages 807-819

  Bonnelle, Valerie ^a   Manohar, Sanjay ^a,b   Behrens, Tim ^a,c   Husain, Masud ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Action initiation; Anterior cingulate cortex; Cingulum bundle; Motivation; Supplementary motor area

Indexed keywords

ADULT; ANTERIOR CINGULATE; APATHY; ARTICLE; BOLD SIGNAL; BRAIN REGION; CINGULATE GYRUS; CONNECTOME; DECISION MAKING; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MOTIVATION; NORMAL HUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; REWARD; SUPPLEMENTARY MOTOR AREA; ASSOCIATION; BRAIN MAPPING; IMAGE PROCESSING; INDIVIDUALITY; MOTOR CORTEX; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOPHYSICS; SELF REPORT; SENSORY FEEDBACK; VASCULARIZATION; WHITE MATTER; YOUNG ADULT;

ADULT; APATHY; BRAIN MAPPING; CUES; DECISION MAKING; FEEDBACK, SENSORY; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; NEURAL PATHWAYS; PHOTIC STIMULATION; PSYCHOPHYSICS; REWARD; SELF REPORT; WHITE MATTER; YOUNG ADULT;

EID: 84960360968     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv247     Document Type: Article

References (74)

1. Adam R, Leff A, Sinha N, Turner C, Bays P, Draganski B, Husain M. 2013. Dopamine reverses reward insensitivity in apathy following globus pallidus lesions. Cortex J Devoted Study Nerv Syst Behav. 49:1292-1303.
2. Apostolova LG, Akopyan GG, Partiali N, Steiner CA, Dutton RA, Hayashi KM, Dinov ID, Toga AW, Cummings JL, Thompson PM. 2007. Structural correlates of apathy in Alzheimer's disease. Dement Geriatr Cogn Disord. 24:91-97.
3. Apps MA, Ramnani N. 2014. The anterior cingulate gyrus signals the net value of others' rewards. J Neurosci. 34:6190-6200.
4. Beckmann CF, Smith SM. 2004. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging. 23:137-152.
5. Beckmann M, Johansen-Berg H, Rushworth MFS. 2009. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci. 29:1175-1190.
6. Behrens TEJ, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CAM, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, et al. 2003. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 6:750-757.
7. Behrens TEJ, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM. 2003. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 50:1077-1088.
8. Bonnelle V, Ham TE, Leech R, Kinnunen KM, Mehta MA, Greenwood RJ, Sharp DJ. 2012. Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci USA. 109:4690-4695.
9. Bonnelle V, Veromann K-R, Burnett Heyes S, Lo Sterzo E, Manohar S, Husain M. 2014. Characterization of reward and effort mechanisms in apathy. J Physiol-Paris. 109:16-26.
10. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. 2001. Conflict monitoring and cognitive control. Psychol Rev. 108:624-652.
11. Botvinick MM, Huffstetler S, McGuire JT. 2009. Effort discounting in human nucleus accumbens. Cogn Affect Behav Neurosci. 9:16-27.
12. Cacciari C, Moraschi M, Di Paola M, Cherubini A, Orfei MD, Giove F, Maraviglia B, Caltagirone C, Spalletta G. 2010. White matter microstructure and apathy level in amnestic mild cognitive impairment. J Alzheimers Dis JAD. 20:501-507.
13. Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 3:201-215.
14. Cowen SL, Davis GA, Nitz DA. 2012. Anterior cingulate neurons in the rat map anticipated effort and reward to their associated action sequences. J Neurophysiol. 107:2393-2407.
15. Croxson PL, Walton ME, O'Reilly JX, Behrens TE, Rushworth MF. 2009. Effort-based cost-benefit valuation and the human brain. J Neurosci Off J Soc Neurosci. 29:4531-4541.
16. Devinsky O, Morrell MJ, Vogt BA. 1995. Contributions of anterior cingulate cortex to behaviour. Brain J Neurol. 118(Pt 1):279-306.
17. Draper A, Stephenson MC, Jackson GM, Pépés S, Morgan PS, Morris PG, Jackson SR. 2014. Increased GABA contributes to enhanced control over motor excitability in Tourette syndrome. Curr Biol. 24:2343-2347.
18. Glimcher PW, Fehr E. 2013. Neuroeconomics: Decision Making and the Brain. London: Academic Press.
19. Grafton ST, Mazziotta JC, Woods RP, Phelps ME. 1992. Human functional anatomy of visually guided finger movements. Brain. 115:565-587.
20. Grinband J,Wager TD, Lindquist M, Ferrera VP, Hirsch J. 2008. Detection of time-varying signals in event-related fMRI designs. NeuroImage. 43:509-520.
21. Hahn C, Lim H-K, Won WY, Ahn KJ, Jung W-S, Lee CU. 2013. Apathy and white matter integrity in Alzheimer's Disease: a whole brain analysis with tract-based spatial statistics. PLoS ONE. 8:e53493.
22. Hare TA, Schultz W, Camerer CF, O'Doherty JP, Rangel A. 2011. Transformation of stimulus value signals into motor commands during simple choice. Proc Natl Acad Sci. 108:18120-18125.
23. Hartmann MN, Hager OM, Tobler PN, Kaiser S. 2013. Parabolic discounting of monetary rewards by physical effort. Behav Process. 100:192-196.
24. Heckhausen J, Heckhausen H. 2010. Motivation and Action. 2nd ed. Cambridge: Cambridge University Press.
25. Holroyd CB, Yeung N. 2012. Motivation of extended behaviors by anterior cingulate cortex. Trends Cogn Sci. 16:122-128.
26. Hosokawa T, Kennerley SW, Sloan J, Wallis JD. 2013. Singleneuron mechanisms underlying cost-benefit analysis in frontal cortex. J Neurosci. 33:17385-17397.
27. Jackson SR, Parkinson A, Kim SY, Schüermann M, Eickhoff SB. 2011. On the functional anatomy of the urge-for-action. Cogn Neurosci. 2:227-243.
28. Jenkinson M, Bannister P, Brady M, Smith S. 2002. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 17:825-841.
29. Jones DK, Catani M, Pierpaoli C, Reeves SJC, Shergill SS, O'Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, et al. 2006. Age effects on diffusion tensormagnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp. 27:230-238.
30. Kable JW, Glimcher PW. 2009. The neurobiology of decision: consensus and controversy. Neuron. 63:733-745.
31. Kerns JG, Cohen JD, MacDonald AW III, Cho RY, Stenger VA, Carter CS. 2004. Anterior cingulate conflict monitoring and adjustments in control. Science. 303:1023-1026.
32. Kostic?VS, Filippi M. 2011. Neuroanatomical correlates of depression and apathy in Parkinson's disease: magnetic resonance imaging studies. J Neurol Sci. 310:61-63.
33. Kurniawan IT, Guitart-Masip M, Dayan P, Dolan RJ. 2013. Effort and valuation in the brain: the effects of anticipation and execution. J Neurosci. 33:6160-6169.
34. Kurniawan IT, Seymour B, Talmi D, Yoshida W, Chater N, Dolan RJ. 2010. Choosing to make an effort: the role of striatum in signaling physical effort of a chosen action. J Neurophysiol. 104:313-321.
35. Lehéricy S, Ducros M, Krainik A, Francois C, Van de Moortele P-F, Ugurbil K, Kim D-S. 2004. 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex. 14:1302-1309.
36. Levy R, Dubois B. 2006. Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex. 16:916-928.
37. Lovibond PF, Lovibond SH. 1995. The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the beck depression and anxiety inventories. Behav Res Ther. 33:335-343.
38. Martino AD, Scheres A, Margulies DS, Kelly AMC, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP. 2008. Functional connectivity of human striatum: a resting state fMRI study. Cereb Cortex. 18:2735-2747.
39. Nachev P, Kennard C, Husain M. 2008. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 9:856-869.
40. Nachev P, Rees G, Parton A, Kennard C, Husain M. 2005. Volition and conflict in human medial frontal cortex. Curr Biol CB. 15:122-128.
41. Nguyen VT, Breakspear M, Cunnington R. 2014. Reciprocal interactions of the SMA and cingulate cortex sustain premovement activity for voluntary actions. J Neurosci. 34:16397-16407.
42. O'Reilly JX, Woolrich MW, Behrens TEJ, Smith SM, Johansen-Berg H. 2012. Tools of the trade: psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci. 7:604-609.
43. Ota M, Sato N, Nakata Y, Arima K, Uno M. 2012. Relationship between apathy and diffusion tensor imaging metrics of the brain in Alzheimer's disease. Int J Geriatr Psychiatry. 27:722-726.
44. Paus T. 2001. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci. 2:417-424.
45. Prévost C, Pessiglione M, Météreau E, Cléry-Melin M-L, Dreher J-C. 2010. Separate valuation subsystems for delay and effort decision costs. J Neurosci. 30:14080-14090.
46. Price CJ, Friston KJ. 1999. Scanning patients with tasks they can perform. Hum Brain Mapp. 8:102-108.
47. Prut Y, Fetz EE. 1999. Primate spinal interneurons show premovement instructed delay activity. Nature. 401:590-594.
48. Radakovic R, Abrahams S. 2014. Developing a new apathy measurement scale: dimensional apathy scale. Psychiatry Res. 219:658-663.
49. Rangel A, Hare T. 2010. Neural computations associated with goal-directed choice. Curr Opin Neurobiol. 20:262-270.
50. Rigoux L, Guigon E. 2012. A model of reward-and effort-based optimal decision making and motor control. PLoS Comput Biol. 8:e1002716.
51. Robert P, Onyike CU, Leentjens AFG, Dujardin K, Aalten P, Starkstein S, Verhey FRJ, Yessavage J, Clement JP, Drapier D, et al. 2009. Proposed diagnostic criteria for apathy in Alzheimer's disease and other neuropsychiatric disorders. Eur Psychiatry J Assoc Eur Psychiatr. 24:98-104.
52. Romo R, SchultzW. 1992. Role of primate basal ganglia and frontal cortex in the internal generation of movements. III. Neuronal activity in the supplementary motor area. Exp Brain Res. 91:396-407.
53. Rushworth MFS, Behrens TEJ. 2008. Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci. 11:389-397.
54. Rushworth MFS, Noonan MP, Boorman ED, Walton ME, Behrens TE. 2011. Frontal cortex and reward-guided learning and decision-making. Neuron. 70:1054-1069.
55. Salamone JD. 2011. A role for accumbens neurons in exertion of effort and evaluating effort-related costs of instrumental actions (Commentary on Day et al.). Eur J Neurosci. 33:306-307.
56. Salamone JD, Correa M, Farrar A, Mingote SM. 2007. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology. 191:461-482.
57. Schmidt L, d'Arc BF, Lafargue G, Galanaud D, Czernecki V, Grabli D, Schüpbach M, Hartmann A, Lévy R, Dubois B, et al. 2008. Disconnecting force from money: effects of basal ganglia damage on incentive motivation. Brain. 131:1303-1310.
58. Shenhav A, Botvinick MM, Cohen JD. 2013. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron. 79:217-240.
59. ShimaK, Tanji J. 1998. Role for cingulatemotor area cells involuntary movement selection based on reward. Science. 282:1335-1338.
60. Snaith RP, Hamilton M, Morley S, Humayan A, Hargreaves D, Trigwell P. 1995. A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. Br J Psychiatry J Ment Sci. 167:99-103.
61. Sockeel P, Dujardin K, Devos D, Denève C, Destée A, Defebvre L. 2006. The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson's disease. J Neurol Neurosurg Psychiatry. 77:579-584.
62. Stanton BR, Leigh PN, Howard RJ, Barker GJ, Brown RG. 2013. Behavioural and emotional symptoms of apathy are associated with distinct patterns of brain atrophy in neurodegenerative disorders. J Neurol. 260:2481-2490.
63. Stuss DT. 2011. Traumatic brain injury: relation to executive dysfunction and the frontal lobes. Curr Opin Neurol. 24:584-589.
64. Stuss DT, Alexander MP. 2007. Is there a dysexecutive syndrome? Philos Trans R Soc B Biol Sci. 362:901-915.
65. Tighe SK, Oishi K, Mori S, Smith GS, Albert M, Lyketsos CG, Mielke MM. 2012. Diffusion tensor imaging of neuropsychiatric symptoms in mild cognitive impairment and Alzheimer's dementia. J Neuropsychiatry Clin Neurosci. 24: 484-488.
66. Treadway MT, Zald DH. 2011. Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci Biobehav Rev. 35:537-555.
67. Vansteenkiste V, Lens W, De Witte H, Feather NT. 2005. UnderstanDing unemployed people's job search behaviour, unemployment experience and well-being: a comparison of expectancy-value theory and self-determination theory. Br J Soc Psychol. 44:269-287.
68. Vergani F, Lacerda L, Martino J, Attems J, Morris C, Mitchell P, Thiebaut de Schotten M, Dell'acqua F. 2014. White matter connections of the supplementary motor area in humans. J Neurol Neurosurg Psychiatry. 85:1377-1385.
69. Vogt BA, Finch DM, Olson CR. 1992. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex. 2:435-443.
70. Walton ME, Bannerman DM, Alterescu K, Rushworth MFS. 2003. Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J Neurosci. 23:6475-6479.
71. Walton M, Kennerley S, Bannerman D, Phillips P, Rushworth M. 2006.Weighing up the benefits of work: behavioral and neural analyses of effort-related decision making. Neural Netw Off J Int Neural Netw Soc. 19:1302-1314.
72. Winstein CJ, Grafton ST, Pohl P.S. 1997.Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography investigation of goal-directed reciprocal aiming using positron emission tomography. J Neurophysiol. 77:1581-1594.
73. Worsley KJ, Evans AC, Marrett S, Neelin P. 1992. A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 12:900-918.
74. Zénon A, Sidibé M, Olivier E. 2015. Disrupting the supplementary motor area makes physical effort appear less effortful. J Neurosci. 35:8737-8744.