Skip to main content
SpringerLink
Log in

Response Hand and Motor Set Differentially Modulate the Connectivity of Brain Pathways During Simple Uni-manual Motor Behavior

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

We investigated the flexible modulation of undirected functional connectivity (uFC) of brain pathways during simple uni-manual responding. Two questions were central to our interests: (1) does response hand (dominant vs. non-dominant) differentially modulate connectivity and (2) are these effects related to responding under varying motor sets. fMRI data were acquired in twenty right-handed volunteers who responded with their right (dominant) or left (non-dominant) hand (blocked across acquisitions). Within acquisitions, the task oscillated between periodic responses (promoting the emergence of motor sets) or randomly induced responses (disrupting the emergence of motor sets). Conjunction analyses revealed eight shared nodes across response hand and condition, time series from which were analyzed. For right hand responses connectivity of the M1 ←→ Thalamus and SMA ←→ Parietal pathways was more significantly modulated during periodic responding. By comparison, for left hand responses, connectivity between five network pairs (including M1 and SMA, insula, basal ganglia, premotor cortex, parietal cortex, thalamus) was more significantly modulated during random responding. uFC analyses were complemented by directed FC based on multivariate autoregressive models of times series from the nodes. These results were complementary and highlighted significant modulation of dFC for SMA → Thalamus, SMA → M1, basal ganglia → Insula and basal ganglia → Thalamus. The results demonstrate complex effects of motor organization and task demand and response hand on different connectivity classes of fMRI data. The brain’s sub-networks are flexibly modulated by factors related to motor organization and/or task demand, and our results have implications for assessment of medical conditions associated with motor dysfunction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abboud R, Noronha C, Diwadkar VA (2017) Motor system dysfunction in the schizophrenia diathesis: neural systems to neurotransmitters. Eur Psychiatry 44:125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adhikari BM, Epstein CM, Dhamala M (2018) Enhanced brain network activity in complex movement rhythms: a simultaneous functional magnetic resonance imaging and electroencephalography study. Brain Connect 8(2):68–81

    Article  PubMed  Google Scholar 

  • Ahissar E, Oram T (2015) Thalamic relay or cortico-thalamic processing? Old question, new answers. Cereb Cortex 25(4):845–848

    Article  PubMed  Google Scholar 

  • Alahmadi AA, Pardini M, Samson RS, D’Angelo E, Friston KJ, Toosy AT et al (2015) Differential involvement of cortical and cerebellar areas using dominant and nondominant hands: an FMRI study. Hum Brain Mapp 36(12):5079–5100

    Article  PubMed  PubMed Central  Google Scholar 

  • Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE et al (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4(3 Pt 1):216–222

    Article  CAS  PubMed  Google Scholar 

  • Ardila A, Bernal B, Rosselli M (2018) Executive functions brain system: an activation likelihood estimation meta-analytic study. Arch Clin Neuropsychol 33(4):379–405

    Article  PubMed  Google Scholar 

  • Asemi A, Ramaseshan K, Burgess A, Diwadkar VA, Bressler SL (2015) Dorsal anterior cingulate cortex modulates supplementary motor area in coordinated unimanual motor behavior. Front Hum Neurosci 9:309

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernard JA, Seidler RD (2012) Hand dominance and age have interactive effects on motor cortical representations. PLoS ONE, 7(9), e45443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bressler SL, Seth AK (2011) Wiener-Granger causality: a well established methodology. Neuroimage 58(2):323–329

    Article  PubMed  Google Scholar 

  • Bressler SL, Tognoli E (2006) Operational principles of neurocognitive networks. Int J Psychophysiol 60(2):139–148

    Article  PubMed  Google Scholar 

  • Bressler SL, Tang W, Sylvester CM, Shulman GL, Corbetta M (2008) Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention. J Neurosci 28(40):10056–10061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan RW, Heinrichs DW (1989) The Neurological Evaluation Scale (NES): a structured instrument for the assessment of neurological signs in schizophrenia. Psychiatry Res 27:335–350

    Article  CAS  PubMed  Google Scholar 

  • Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA et al (1998) A common network of functional areas for attention and eye movements. Neuron 21(4):761–773

    Article  CAS  PubMed  Google Scholar 

  • Cunnington R, Windischberger C, Deecke L, Moser E (2003) The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 20(1):404–412

    Article  PubMed  Google Scholar 

  • Diwadkar VA, Murphy ER, Freedman RR (2014) Temporal sequencing of brain activations during naturally occurring thermoregulatory events. Cereb Cortex 24:3006–3013

    Article  PubMed  Google Scholar 

  • Diwadkar VA, Asemi A, Burgess A, Chowdury A, Bressler SL (2017a) Potentiation of motor sub-networks for motor control but not working memory: interaction of dACC and SMA revealed by resting-state directed functional connectivity. PLoS ONE, 12(3), e0172531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diwadkar VA, Bellani M, Chowdury A, Savazzi S, Perlini C, Marinelli V et al (2017b) Activations in gray and white matter are modulated by uni-manual responses during within and inter-hemispheric transfer: effects of response hand and right-handedness. Brain Imaging Behav. https://doi.org/10.1007/s11682-017-9750-7

    Article  Google Scholar 

  • Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361

    Article  PubMed  Google Scholar 

  • First MD, Gibbon M, Spitzer RL, Williams JBW, Benjamin LS (1997) Structured clinical interview for DSM-IV axis II personality disorders. Biometrics Research Department, NYSPI, New York

    Google Scholar 

  • Fogassi L, Luppino G (2005) Motor functions of the parietal lobe. Curr Opin Neurobiol 15(6):626–631

    Article  CAS  PubMed  Google Scholar 

  • Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308(5722):662–667

    Article  CAS  PubMed  Google Scholar 

  • Friedman A, Burgess A, Ramaseshan K, Easter P, Khatib D, Chowdury A et al (2017) Brain network dysfunction in obsessive-compulsive disorder induced by simple uni-manual behavior: the role of the dorsal anterior cingulate cortex. Psychiatry Res Neuroimaging 260:6–15

    Article  PubMed  Google Scholar 

  • Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1(1):13–36

    Article  PubMed  Google Scholar 

  • Gao Q, Duan X, Chen H (2011) Evaluation of effective connectivity of motor areas during motor imagery and execution using conditional Granger causality. Neuroimage 54(2):1280–1288

    Article  PubMed  Google Scholar 

  • Ghaziri J, Tucholka A, Girard G, Houde JC, Boucher O, Gilbert G et al (2017) The corticocortical structural connectivity of the human insula. Cereb Cortex 27(2):1216–1228

    Article  PubMed  Google Scholar 

  • Goble DJ, Coxon JP, Van Impe A, De Vos J, Wenderoth N, Swinnen SP (2010) The neural control of bimanual movements in the elderly: brain regions exhibiting age-related increases in activity, frequency-induced neural modulation, and task-specific compensatory recruitment. Hum Brain Mapp 31(8):1281–1295

    PubMed  Google Scholar 

  • Goense JB, Logothetis NK (2008) Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol 18(9):631–640

    Article  CAS  PubMed  Google Scholar 

  • Grafton ST, Mazziotta JC, Woods RP, Phelps ME (1992) Human functional anatomy of visually guided finger movements. Brain 115(Pt 2):565–587

    Article  PubMed  Google Scholar 

  • Grafton ST, Hazeltine E, Ivry RB (2002) Motor sequence learning with the nondominant left hand. A PET functional imaging study. Exp Brain Res 146(3):369–378

    Article  PubMed  Google Scholar 

  • Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR (2008) Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 41(4):1382–1394

    Article  PubMed  Google Scholar 

  • Guo Y, Schmitz TW, Mur M, Ferreira CS, Anderson MC (2017) A supramodal role of the basal ganglia in memory and motor inhibition: meta-analytic evidence. Neuropsychologia 108:117–134

    Article  PubMed  Google Scholar 

  • Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, Salek-Haddadi A et al (2003) Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 19(4):1349–1360

    Article  PubMed  Google Scholar 

  • Haaland KY, Harrington DL, Knight RT (2000) Neural representations of skilled movement. Brain 123(Pt 11):2306–2313

    Article  PubMed  Google Scholar 

  • Haaland KY, Elsinger CL, Mayer AR, Durgerian S, Rao SM (2004) Motor sequence complexity and performing hand produce differential patterns of hemispheric lateralization. J Cogn Neurosci 16(4):621–636

    Article  PubMed  Google Scholar 

  • Hoffstaedter F, Grefkes C, Caspers S, Roski C, Palomero-Gallagher N, Laird AR et al (2014) The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum Brain Mapp 35(6):2741–2753

    Article  PubMed  Google Scholar 

  • Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Stimulus-dependent BOLD and perfusion dynamics in human V1. Neuroimage 9(6 Pt 1):573–585

    Article  CAS  PubMed  Google Scholar 

  • Jagtap P, Diwadkar VA (2016) Effective connectivity of ascending and descending frontalthalamic pathways during sustained attention: complex brain network interactions in adolescence. Hum Brain Mapp 37(7):2557–2570

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SG, Ashe J, Hendrich K, Ellermann JM, Merkle H, Ugurbil K et al (1993) Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science 261(5121):615–617

    Article  CAS  PubMed  Google Scholar 

  • Kolodny T, Mevorach C, Shalev L (2017) Isolating response inhibition in the brain: parietal versus frontal contribution. Cortex 88:173–185

    Article  PubMed  Google Scholar 

  • Lehericy S, Bardinet E, Tremblay L, Van de Moortele PF, Pochon JB, Dormont D et al (2006) Motor control in basal ganglia circuits using fMRI and brain atlas approaches. Cereb Cortex 16(2):149–161

    Article  PubMed  Google Scholar 

  • Liepmann H (1905) The left hemisphere and action. Republished in 1908 in Drei Aufsatze aus dem Apraxiegebiet. Karger, Berlin

  • Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453(7197):869–878

    Article  CAS  PubMed  Google Scholar 

  • Lotze M, Erb M, Flor H, Huelsmann E, Godde B, Grodd W (2000) fMRI evaluation of somatotopic representation in human primary motor cortex. Neuroimage 11(5 Pt 1):473–481

    Article  CAS  PubMed  Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239

    Article  PubMed  Google Scholar 

  • Mesulam MM (1998) From sensation to cognition. Brain 121:1013–1052

    Article  PubMed  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    Article  CAS  PubMed  Google Scholar 

  • Muzik O, Diwadkar VA (2016) In vivo correlates of thermoregulatory defense in humans: temporal course of sub-cortical and cortical responses assessed with fMRI. Hum Brain Mapp 37(9):3188–3202

    Article  PubMed  Google Scholar 

  • Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869

    Article  CAS  PubMed  Google Scholar 

  • Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25(3):653–660

    Article  PubMed  Google Scholar 

  • Nuber S, Petrasch-Parwez E, Winner B, Winkler J, von Horsten S, Schmidt T et al (2008) Neurodegeneration and motor dysfunction in a conditional model of Parkinson’s disease. J Neurosci 28(10):2471–2484

    Article  CAS  PubMed  Google Scholar 

  • Park HJ, Friston K (2013) Structural and functional brain networks: from connections to cognition. Science 342(6158):1238411

    Article  CAS  PubMed  Google Scholar 

  • Passingham RE, Stephan KE, Kotter R (2002) The anatomical basis of functional localization in the cortex. Nat Rev Neurosci 3(8):606–616

    Article  CAS  PubMed  Google Scholar 

  • Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2(6):417–424

    Article  CAS  PubMed  Google Scholar 

  • Pool EM, Rehme AK, Fink GR, Eickhoff SB, Grefkes C (2014) Handedness and effective connectivity of the motor system. Neuroimage 99:451–460

    Article  PubMed  PubMed Central  Google Scholar 

  • Pool EM, Rehme AK, Eickhoff SB, Fink GR, Grefkes C (2015) Functional resting-state connectivity of the human motor network: differences between right- and left-handers. Neuroimage 109:298–306

    Article  PubMed  PubMed Central  Google Scholar 

  • Pool EM, Leimbach M, Binder E, Nettekoven C, Eickhoff SB, Fink GR et al (2018) Network dynamics engaged in the modulation of motor behavior in stroke patients. Hum Brain Mapp 39(3):1078–1092

    Article  PubMed  Google Scholar 

  • Price CJ, Friston KJ (2005) Functional ontologies for cognition: the systematic definition of structure and function. Cogn Neuropsychol 22(3):262–275

    Article  PubMed  Google Scholar 

  • Rathelot JA, Dum RP, Strick PL (2017) Posterior parietal cortex contains a command apparatus for hand movements. Proc Natl Acad Sci USA 114(16):4255–4260

    Article  CAS  PubMed  Google Scholar 

  • Saalmann YB, Kastner S (2011) Cognitive and perceptual functions of the visual thalamus. Neuron 71(2):209–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sale MV, Reid LB, Cocchi L, Pagnozzi AM, Rose SE, Mattingley JB (2017) Brain changes following four weeks of unimanual motor training: evidence from behavior, neural stimulation, cortical thickness, and functional MRI. Hum Brain Mapp 38(9):4773–4787

    Article  PubMed  Google Scholar 

  • Sarfeld AS, Diekhoff S, Wang LE, Liuzzi G, Uludag K, Eickhoff SB et al (2012) Convergence of human brain mapping tools: neuronavigated TMS parameters and fMRI activity in the hand motor area. Hum Brain Mapp 33(5):1107–1123

    Article  PubMed  Google Scholar 

  • Seizeur R, Magro E, Prima S, Wiest-Daessle N, Maumet C, Morandi X (2014) Corticospinal tract asymmetry and handedness in right- and left-handers by diffusion tensor tractography. Surg Radiol Anat 36(2):111–124

    Article  PubMed  Google Scholar 

  • Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9(4):569–577

    Article  CAS  PubMed  Google Scholar 

  • Silverstein B, Bressler S, Diwadkar VA (2016) Inferring the dysconnection syndrome in schizophrenia: interpretational considerations on methods for the network analyses of fMRI data. Front Psychiatry 7:132

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh KD (2012) Which “neural activity” do you mean? fMRI, MEG, oscillations and neurotransmitters. Neuroimage 62(2):1121–1130

    Article  PubMed  Google Scholar 

  • Singh LN, Higano S, Takahashi S, Kurihara N, Furuta S, Tamura H et al (1998) Comparison of ipsilateral activation between right and left handers: a functional MR imaging study. Neuroreport 9(8):1861–1866

    Article  CAS  PubMed  Google Scholar 

  • Sisti HM, Geurts M, Clerckx R, Gooijers J, Coxon JP, Heitger MH et al (2011) Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS ONE, 6(8), e23619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang W, Bressler SL, Sylvester CM, Shulman GL, Corbetta M (2012) Measuring Granger causality between cortical regions from voxelwise fMRI BOLD signals with LASSO. PLoS Comput Biol, 8(5), e1002513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanji J (1994) The supplementary motor area in the cerebral cortex. Neurosci Res 19(3):251–268

    Article  CAS  PubMed  Google Scholar 

  • Tomasino B, Gremese M (2016) The cognitive side of M1. Front Hum Neurosci 10:298

    Article  PubMed  PubMed Central  Google Scholar 

  • Tootell RB, Mendola JD, Hadjikhani NK, Liu AK, Dale AM (1998) The representation of the ipsilateral visual field in human cerebral cortex. Proc Natl Acad Sci USA 95(3):818–824

    Article  CAS  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Petit L, Zago L, Crivello F, Vinuesa N, Joliot M et al (2015) Between-hand difference in ipsilateral deactivation is associated with hand lateralization: fMRI mapping of 284 volunteers balanced for handedness. Front Hum Neurosci 9:5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uddin LQ, Nomi JS, Hebert-Seropian B, Ghaziri J, Boucher O (2017) Structure and function of the human insula. J Clin Neurophysiol 34(4):300–306

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Berg FE, Swinnen SP, Wenderoth N (2011) Involvement of the primary motor cortex in controlling movements executed with the ipsilateral hand differs between left- and right-handers. J Cogn Neurosci 23(11):3456–3469

    Article  PubMed  Google Scholar 

  • Velikova S, Locatelli M, Insacco C, Smeraldi E, Comi G, Leocani L (2010) Dysfunctional brain circuitry in obsessive-compulsive disorder: source and coherence analysis of EEG rhythms. Neuroimage 49(1):977–983

    Article  PubMed  Google Scholar 

  • Volkmann J, Schnitzler A, Witte OW, Freund H (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79(4):2149–2154

    Article  CAS  PubMed  Google Scholar 

  • Ward BD (2000) Simultaneous inference for fMRI data. Medical College of Wisconsin, Milwaukee, WI

    Google Scholar 

  • Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2(3):125–141

    Article  PubMed  Google Scholar 

  • Witt ST, Stevens MC (2013) The role of top-down control in different phases of a sensorimotor timing task: a DCM study of adults and adolescents. Brain Imaging Behav 7(3):260–273

    Article  PubMed  Google Scholar 

  • Witt ST, Laird AR, Meyerand ME (2008) Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. Neuroimage 42(1):343–356

    Article  PubMed  PubMed Central  Google Scholar 

  • Zapparoli L, Seghezzi S, Paulesu E (2017) The what, the when, and the whether of intentional action in the brain: a meta-analytical review. Front Hum Neurosci 11:238

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Preparation of this work was supported by a Career Development Chair from Wayne State University, the Charles H. Gershenson Distinguished Faculty Fellowship from Wayne State University, the Lyckaki-Young Fund from the State of Michigan, the Prechter Family Bipolar Foundation, the Children’s Hospital of Michigan Foundation, the Children’s Research Center of Michigan, the Cohen Neuroscience Endowment, the Dorsey Endowment, a Medical Student Internship from the Detroit Medical Center, and the National Institute of Mental Health (MH 59299).

Author information

Authors and Affiliations

  1. Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Suite 5A, Tolan Park Medical Building, 3901 Chrysler Service Drive, Detroit, MI, 48201, USA

    Alexandra Morris, Mathura Ravishankar, Lena Pivetta, Asadur Chowdury, David R. Rosenberg & Vaibhav A. Diwadkar

  2. Center for Complex Systems and Brain Sciences, Florida Atlantic University, Boca Raton, USA

    Dimitri Falco & Steven L. Bressler

  3. Department of Psychology, Wayne State University, Detroit, USA

    Jessica S. Damoiseaux

  4. Institute of Gerontology, Wayne State University, Detroit, USA

    Jessica S. Damoiseaux

Authors
  1. Alexandra Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mathura Ravishankar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lena Pivetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Asadur Chowdury
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dimitri Falco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jessica S. Damoiseaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David R. Rosenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Steven L. Bressler
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Vaibhav A. Diwadkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vaibhav A. Diwadkar.

Additional information

Handling Editor: Fabrizio De Vico Fallani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morris, A., Ravishankar, M., Pivetta, L. et al. Response Hand and Motor Set Differentially Modulate the Connectivity of Brain Pathways During Simple Uni-manual Motor Behavior. Brain Topogr 31, 985–1000 (2018). https://doi.org/10.1007/s10548-018-0664-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-018-0664-5

Keywords

Search

Navigation