Decreased neural activity and neural connectivity while performing a set-shifting task after inhibiting repetitive transcranial magnetic stimulation on the left dorsal prefrontal cortex

BMC Neuroscience

Ysbrand D van der Werf¹  Odile A van den Heuvel¹  Niels J H M Gerrits¹ 

[1] Neuroscience Campus Amsterdam (NCA), Amsterdam, The Netherlands

关键词: Connectivity;    Prefrontal cortex;    Functional magnetic resonance imaging;    Low-frequency repetitive transcranial magnetic stimulation;    Set-shifting;    Key-words;   

Others  :  1220304
DOI  :  10.1186/s12868-015-0181-3

 received in 2014-12-11, accepted in 2015-07-13,  发布年份 2015

【 摘 要 】

Background

Sub-optimal functioning of the dorsal prefrontal cortex (PFC) is associated with executive dysfunction, such as set-shifting deficits, in neurological and psychiatric disorders. We tested this hypothesis by investigating the effect of low-frequency ‘inhibiting’ off-line repetitive transcranial magnetic stimulation (rTMS) on the left dorsal prefrontal cortex on behavioural performance, neural activity, and network connectivity during the performance of a set-shifting paradigm in healthy elderly (mean age 50+).

Results

Behaviorally, we found a group-by-session interaction for errors on set-shift trials, although post hoc tests did not yield significant findings. In addition, the verum group, when compared with the sham group, displayed reduced task-related activity in the left temporal gyrus, and reduced task-related connectivity of the left PFC with the left postcentral gyrus and posterior insula.

Conclusion

These results show that low-frequency off-line rTMS on the left dorsal PFC resulted in reduced task-related activity and network connectivity, which was accompanied by a subtle behavioural effect, thereby further corroborating the importance of an optimally functioning PFC in set-shifting.

【 授权许可】

   
2015 Gerrits et al.

【 图 表 】

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【 参考文献 】

• [1]Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS: Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 2012, 12(2):241-268.
• [2]Monsell S: Task switching. Trends Cogn Sci 2003, 7(3):134-140.
• [3]van den Heuvel OA, Veltman DJ, Groenewegen HJ, Cath DC, van Balkom AJ, van Hartskamp J, et al.: Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. Arch Gen Psychiatry 2005, 62(3):301-309.
• [4]Quide Y, Morris RW, Shepherd AM, Rowland JE, Green MJ: Task-related fronto-striatal functional connectivity during working memory performance in schizophrenia. Schizophr Res 2013, 150(2–3):468-475.
• [5]Grahn JA, Parkinson JA, Owen AM: The role of the basal ganglia in learning and memory: neuropsychological studies. Behav Brain Res 2009, 199(1):53-60.
• [6]Monchi O, Petrides M, Mejia-Constain B, Strafella AP: Cortical activity in Parkinson’s disease during executive processing depends on striatal involvement. Brain 2007, 130(Pt 1):233-244.
• [7]Hallett M: Transcranial magnetic stimulation: a primer. Neuron 2007, 55(2):187-199.
• [8]Muellbacher W, Ziemann U, Boroojerdi B, Hallett M: Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 2000, 111(6):1002-1007.
• [9]Touge T, Gerschlager W, Brown P, Rothwell JC: Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 2001, 112(11):2138-2145.
• [10]Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J: BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage 2005, 28(1):22-29.
• [11]Valero-Cabre A, Payne BR, Pascual-Leone A: Opposite impact on 14C-2-deoxyglucose brain metabolism following patterns of high and low frequency repetitive transcranial magnetic stimulation in the posterior parietal cortex. Exp Brain Res 2007, 176(4):603-615.
• [12]Ruff CC, Driver J, Bestmann S: Combining TMS and fMRI: from ‘virtual lesions’ to functional-network accounts of cognition. Cortex 2009, 45(9):1043-1049.
• [13]Sandrini M, Umilta C, Rusconi E: The use of transcranial magnetic stimulation in cognitive neuroscience: a new synthesis of methodological issues. Neurosci Biobehav Rev 2011, 35(3):516-536.
• [14]van den Heuvel OA, Van Gorsel HC, Veltman DJ, Van Der Werf YD: Impairment of executive performance after transcranial magnetic modulation of the left dorsal frontal-striatal circuit. Hum Brain Mapp 2013, 34(2):347-355.
• [15]Fox MD, Halko MA, Eldaief MC, Pascual-Leone A: Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). Neuroimage 2012, 62(4):2232-2243.
• [16]Fox MD, Buckner RL, White MP, Greicius MD, Pascual-Leone A: Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biol Psychiatry 2012, 72(7):595-603.
• [17]Paus T, Castro-Alamancos MA, Petrides M: Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci 2001, 14(8):1405-1411.
• [18]Akam T, Kullmann DM: Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat Rev Neurosci 2014, 15(2):111-122.
• [19]Buzsaki G, Draguhn A: Neuronal oscillations in cortical networks. Science 2004, 304(5679):1926-1929.
• [20]Uhlhaas PJ, Singer W: Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 2012, 75(6):963-980.
• [21]Grant DA, Berg EA: A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. J Exp Psychol 1948, 38(4):404-411.
• [22]Cools R, Barker RA, Sahakian BJ, Robbins TW: Mechanisms of cognitive set flexibility in Parkinson’s disease. Brain 2001, 124(Pt 12):2503-2512.
• [23]Rogers RD, Monsell S: Costs of a predictable switch between simple cognitive tasks. J Exp Psychol 1995, 124(2):207-231.
• [24]Koch I: The role of external cues for endogenous advance reconfiguration in task switching. Psychon Bull Rev 2003, 10(2):488-492.
• [25]Kiesel A, Steinhauser M, Wendt M, Falkenstein M, Jost K, et al.: Control and interference in task switching—a review. Psychol Bull 2010, 136(5):849-874.
• [26]Buchsbaum BR, Greer S, Chang WL, Berman KF: Meta-analysis of neuroimaging studies of the Wisconsin card-sorting task and component processes. Hum Brain Mapp 2005, 25(1):35-45.
• [27]Wager TD, Jonides J, Reading S: Neuroimaging studies of shifting attention: a meta-analysis. Neuroimage 2004, 22(4):1679-1693.
• [28]Kim C, Cilles SE, Johnson NF, Gold BT: Domain general and domain preferential brain regions associated with different types of task switching: a meta-analysis. Hum Brain Mapp 2012, 33(1):130-142.
• [29]van der Werf YD, Sanz-Arigita EJ, Menning S, van den Heuvel OA: Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation. BMC Neurosci 2011, 11:145. BioMed Central Full Text
• [30]Raichle ME, Snyder AZ: A default mode of brain function: a brief history of an evolving idea. Neuroimage 2007, 37(4):1083-1090.
• [31]Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL: A default mode of brain function. Proc Natl Acad Sci USA 2001, 98(2):676-682.
• [32]Greicius MD, Menon V: Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. J Cogn Neurosci 2004, 16(9):1484-1492.
• [33]Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS: Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 2013, 16(9):1348-1355.
• [34]Brunoni AR, Vanderhasselt MA: Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: a systematic review and meta-analysis. Brain Cogn 2014, 86:1-9.
• [35]Boroojerdi B, Meister IG, Foltys H, Sparing R, Cohen LG, Topper R: Visual and motor cortex excitability: a transcranial magnetic stimulation study. Clin Neurophysiol 2002, 113(9):1501-1504.
• [36]Gerrits NJ, van der Werf YD, Verhoef KM, Veltman DJ, Groenewegen HJ, Berendse HW, et al.: Compensatory fronto-parietal hyperactivation during set-shifting in unmedicated patients with Parkinson’s disease. Neuropsychologia 2015, 68:107-116.
• [37]Spitzer RL, Williams JB, Gibbon M, First MB: The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. Arch Gen Psychiatry 1992, 49(8):624-629.
• [38]Beck AT, Steer RA, Ball R, Ranieri W: Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess 1996, 67(3):588-597.
• [39]Beck AT, Epstein N, Brown G, Steer RA: An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 1988, 56(6):893-897.
• [40]Cockrell JR, Folstein MF: Mini-Mental State Examination (MMSE). Psychopharmacol Bull 1988, 24(4):689-692.
• [41]Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9(1):97-113.
• [42]Sack AT, Cohen Kadosh R, Schuhmann T, Moerel M, Walsh V, Goebel R: Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci 2009, 21(2):207-221.
• [43]Hoogendam JM, Ramakers GM, Di Lazzaro V: Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010, 3(2):95-118.
• [44]Ridding MC, Ziemann U: Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 2010, 588(Pt 13):2291-2304.
• [45]Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH: An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19(3):1233-1239.
• [46]McLaren DG, Ries ML, Xu G, Johnson SC: A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 2012, 61(4):1277-1286.
• [47]O’Reilly JX, Woolrich MW, Behrens TE, Smith SM, Johansen-Berg H: Tools of the trade: psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci 2012, 7(5):604-609.