Abstract
Some pain-related information is processed preferentially in the right cerebral hemisphere. Considering that functional lateralization can be affected by handedness, spinal and cerebral pain-related responses may be different between right- and left-handed individuals. Therefore, this study aimed to investigate the cortical and spinal mechanisms of nociceptive integration when nociceptive stimuli are applied to right -handed vs. left -handed individuals. The NFR, evoked potentials (ERP: P45, N100, P260), and event-related spectral perturbations (ERSP: theta, alpha, beta and gamma band oscillations) were compared between ten right-handed and ten left-handed participants. Pain was induced by transcutaneous electrical stimulation of the lower limbs and left upper limb. Stimulation intensity was adjusted individually in five counterbalanced conditions of 21 stimuli each: three unilateral (right lower limb, left lower limb, and left upper limb stimulation) and two bilateral conditions (right and left lower limbs, and the right lower limb and left upper limb stimulation). The amplitude of the NFR, ERP, ERSP, and pain ratings were compared between groups and conditions using a mixed ANOVA. A significant increase of responses was observed in bilateral compared with unilateral conditions for pain intensity, NFR amplitude, N100, theta oscillations, and gamma oscillations. However, these effects were not significantly different between right- and left-handed individuals. These results suggest that spinal and cerebral integration of bilateral nociceptive inputs is similar between right- and left-handed individuals. They also imply that pain-related responses measured in this study may be examined independently of handedness.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The datasets generated during the current study are available from the corresponding author on reasonable request.
Code availability
The codes generated during the current study are available from the corresponding author on reasonable request.
References
Aimonetti J-M, Morin D, Schmied A, Vedel J-P, Pagni S (1999) Proprioceptive control of wrist extensor motor units in humans: dependence on handedness. Somatosens Mot Res 16(1):11–29. https://doi.org/10.1080/08990229970618
Aloisi AM (2017) Why we still need to speak about sex differences and sex hormones in pain. Pain Ther 6(2):111–114. https://doi.org/10.1007/s40122-017-0084-3
Antonaci F, Bovim G, Fasano ML, Bonamico L, Shen JM (1992) Pain threshold in humans. A study with the pressure algometer. Funct Neurol 7(4):283–288
Arendt-Nielsen L, Sonnenborg FA, Andersen OK (2000) Facilitation of the withdrawal reflex by repeated transcutaneous electrical stimulation: an experimental study on central integration in humans. Eur J Appl Physiol 81(3):165–173. https://doi.org/10.1007/s004210050026
Bingel U, Quante M, Knab R, Bromm B, Weiller C, Büchel C (2003) Single trial fMRI reveals significant contralateral bias in responses to laser pain within thalamus and somatosensory cortices. Neuroimage 18(3):740–748. https://doi.org/10.1016/s1053-8119(02)00033-2
Brennum J, Kjeldsen M, Jensen K, Jensen TS (1989) Measurements of human pressure-pain thresholds on fingers and toes. Pain 38(2):211–217. https://doi.org/10.1016/0304-3959(89)90240-6
Broca P (1863) Localisations des fonctions cérébrales. Siège de la faculté du language articulé. Bulletin De La Société D’anthropologie 4:200–208
Brooks JC, Nurmikko TJ, Bimson WE, Singh KD, Roberts N (2002) fMRI of thermal pain: effects of stimulus laterality and attention. Neuroimage 15(2):293–301
Bryden MP, Hécaen H, DeAgostini M (1983) Patterns of cerebral organization. Brain Lang 20(2):249–262. https://doi.org/10.1016/0093-934x(83)90044-5
Bryden PJ, Mayer M, Roy EA (2011) Influences of task complexity, object location, and object type on hand selection in reaching in left and right-handed children and adults. Dev Psychobiol 53(1):47–58. https://doi.org/10.1002/dev.20486
Buchanan HM, Midgley JA (1987) Evaluation of pain threshold using a simple pressure algometer. Clin Rheumatol 6(4):510–517. https://doi.org/10.1007/bf02330587
Burke KA, Letsos A, Butler RA (1994) Asymmetric performances in binaural localization of sound in space. Neuropsychologia 32(11):1409–1417. https://doi.org/10.1016/0028-3932(94)00074-3
Cai Q, Van der Haegen L, Brysbaert M (2013) Complementary hemispheric specialization for language production and visuospatial attention. Proc Natl Acad Sci 110(4):E322–E330. https://doi.org/10.1073/pnas.1212956110
Cazzoli D, Chechlacz M (2017) A matter of hand: Causal links between hand dominance, structural organization of fronto-parietal attention networks, and variability in behavioural responses to transcranial magnetic stimulation. Cortex 86:230–246. https://doi.org/10.1016/j.cortex.2016.06.015
Chechlacz M, Gillebert CR, Vangkilde SA, Petersen A, Humphreys GW (2015) Structural variability within frontoparietal networks and individual differences in attentional functions: an approach using the theory of visual attention. J Neurosci 35(30):10647–10658. https://doi.org/10.1523/jneurosci.0210-15.2015
Chéry-Croze S (1983) Relationship between noxious cold stimuli and the magnitude of pain sensation in man. Pain 15(3):265–269. https://doi.org/10.1016/0304-3959(83)90061-1
Coghill RC, Gilron I, Iadarola MJ (2001) Hemispheric lateralization of somatosensory processing. J Neurophysiol 85(6):2602–2612. https://doi.org/10.1152/jn.2001.85.6.2602
Corballis MC (2009) The evolution and genetics of cerebral asymmetry. Philos Trans R Soc Lond B Biol Sci 364(1519):867–879. https://doi.org/10.1098/rstb.2008.0232
Corballis MC (2014) Left brain, right brain: facts and fantasies. PLoS Biol 12(1):e1001767. https://doi.org/10.1371/journal.pbio.1001767
Corballis MC (2020) Bilaterally symmetrical: to be or not to be? Symmetry 12(3):326
Corballis MC, Häberling IS (2017) The many sides of hemispheric asymmetry: a selective review and outlook. J Int Neuropsychol Soc 23(9–10):710–718. https://doi.org/10.1017/s1355617717000376
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215. https://doi.org/10.1038/nrn755
Cykowski MD, Coulon O, Kochunov PV, Amunts K, Lancaster JL, Laird AR, Fox PT (2008) The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. Cereb Cortex 18(9):1999–2009. https://doi.org/10.1093/cercor/bhm224
De Renzi, E. (1978). Hemispheric asymmetry as evidenced by spatial disorders. Asymmetrical function of the brain, 49–85.
De Renzi, E. (1982). Disorders of space exploration and cognition. JOHN WILEY & SONS, INC., 605 THIRD AVE., NEW YORK, NY 10158. 1982.
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Dowman R (1994) SEP topographies elicited by innocuous and noxious sural nerve stimulation I Identification of stable periods and individual differences. Electroencephalog Clin Neurophysiol/evoked Potentials Sect 92(4):291–302. https://doi.org/10.1016/0168-5597(94)90097-3
Dowman R (2004a) Distraction produces an increase in pain-evoked anterior cingulate activity. Psychophysiology 41(4):613–624. https://doi.org/10.1111/1469-8986.00186.x
Dowman R (2004b) The pain-evoked P2 is not a P3a event-related potential. Brain Topogr 17(1):3–12. https://doi.org/10.1023/b:brat.0000047332.24629.8e
Dowman R (2004c) Topographic analysis of painful laser and sural nerve electrical evoked potentials. Brain Topogr 16(3):169–179. https://doi.org/10.1023/b:brat.0000019185.30489.ad
Dowman R, Darcey T, Barkan H, Thadani V, Roberts D (2007) Human intracranially-recorded cortical responses evoked by painful electrical stimulation of the sural nerve. Neuroimage 34(2):743–763. https://doi.org/10.1016/j.neuroimage.2006.09.021
Driver J, Grossenbacher PG (1996) Multimodal spatial constraints on tactile selective attention Attention and performance 16: Information integration in perception and communication. The MIT Press, Cambridge, MA, US, pp 209–235
Duboc V, Dufourcq P, Blader P, Roussigne M (2015) Asymmetry of the brain: development and implications. Annu Rev Genet 49:647–672. https://doi.org/10.1146/annurev-genet-112414-055322
Duerden EG, Albanese MC (2013) Localization of pain-related brain activation: a meta-analysis of neuroimaging data. Hum Brain Mapp 34(1):109–149. https://doi.org/10.1002/hbm.21416
Duquette M, Rainville P, Alary F, Lassonde M, Lepore F (2008) Ipsilateral cortical representation of tactile and painful information in acallosal and callosotomized subjects. Neuropsychologia 46(8):2274–2279. https://doi.org/10.1016/j.neuropsychologia.2008.02.017
Ehret G (1987) Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls. Nature 325(6101):249–251. https://doi.org/10.1038/325249a0
Fischer AA (1987) Pressure algometry over normal muscles. Standard values, validity and reproducibility of pressure threshold. Pain 30(1):115–126. https://doi.org/10.1016/0304-3959(87)90089-3
Flöel A, Buyx A, Breitenstein C, Lohmann H, Knecht S (2005) Hemispheric lateralization of spatial attention in right- and left-hemispheric language dominance. Behav Brain Res 158(2):269–275. https://doi.org/10.1016/j.bbr.2004.09.016
Fouché JJ, Van Loghem JAJ, Thuis J, De Heer LM, van Oijen MGH (2017) Left/right pain asymmetry with injectable cosmetic treatments for the face. Aesthet Surg J 37(6):708–714. https://doi.org/10.1093/asj/sjw214
Friston KJ (2005) Models of brain function in neuroimaging. Annu Rev Psychol 56:57–87. https://doi.org/10.1146/annurev.psych.56.091103.070311
Gazzaniga MS (2005) Forty-five years of split-brain research and still going strong. Nat Rev Neurosci 6(8):653–659. https://doi.org/10.1038/nrn1723
Gazzaniga MS, Bogen JE, Sperry RW (1962) Some functional effects of sectioning the cerebral commissures in man. Proc Natl Acad Sci U S A 48(10):1765–1769. https://doi.org/10.1073/pnas.48.10.1765
Geschwind N, Levitsky W (1968) Human brain: left-right asymmetries in temporal speech region. Science 161(3837):186–187. https://doi.org/10.1126/science.161.3837.186
Geuze RH, Schaafsma SM, Lust JM, Bouma A, Schiefenhövel W, Groothuis TG (2012) Plasticity of lateralization: schooling predicts hand preference but not hand skill asymmetry in a non-industrial society. Neuropsychologia 50(5):612–620. https://doi.org/10.1016/j.neuropsychologia.2011.12.017
Gilbert AN, Wysocki CJ (1992) Hand preference and age in the United States. Neuropsychologia 30(7):601–608. https://doi.org/10.1016/0028-3932(92)90065-t
Gilmore CS, Clementz BA, Berg P (2009) Hemispheric differences in auditory oddball responses during monaural versus binaural stimulation. Int J Psychophysiol 73(3):326–333. https://doi.org/10.1016/j.ijpsycho.2009.05.005
Goldberg E, Podell K, Lovell M (1994) Lateralization of frontal lobe functions and cognitive novelty. J Neuropsychiatry Clin Neurosci 6(4):371–378. https://doi.org/10.1176/jnp.6.4.371
Gonzalez CLR, van Rootselaar NA, Gibb RL (2018) Sensorimotor lateralization scaffolds cognitive specialization. Prog Brain Res 238:405–433. https://doi.org/10.1016/bs.pbr.2018.06.011
Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci U S A 110(36):E3435-3444. https://doi.org/10.1073/pnas.1302581110
Greenspan JD, McGillis SL (1994) Thresholds for the perception of pressure, sharpness, and mechanically evoked cutaneous pain: effects of laterality and repeated testing. Somatosens Mot Res 11(4):311–317. https://doi.org/10.3109/08990229409028875
Greenspan JD, Taylor DJ, McGillis SL (1993) Body site variation of cool perception thresholds, with observations on paradoxical heat. Somatosens Mot Res 10(4):467–474. https://doi.org/10.3109/08990229309028851
Haaland KY, Harrington DL, Knight RT (2000) Neural representations of skilled movement. Brain 123(Pt 11):2306–2313. https://doi.org/10.1093/brain/123.11.2306
Hagbarth KE (1960) Spinal withdrawal reflexes in the human lower limbs. J Neurol Neurosurg Psychiatry 23(3):222–227. https://doi.org/10.1136/jnnp.23.3.222
Hammond G (2002) Correlates of human handedness in primary motor cortex: a review and hypothesis. Neurosci Biobehav Rev 26(3):285–292. https://doi.org/10.1016/s0149-7634(02)00003-9
Haslam DR (1970) Lateral dominance in the perception of size and of pain. Q J Exp Psychol 22(3):503–507. https://doi.org/10.1080/14640747008401926
Hauck M, Lorenz J, Engel AK (2007) Attention to painful stimulation enhances γ-band activity and synchronization in human sensorimotor cortex. J Neurosci 27(35):9270–9277. https://doi.org/10.1523/jneurosci.2283-07.2007
Hauck M, Domnick C, Lorenz J, Gerloff C, Engel AK (2015) Top-down and bottom-up modulation of pain-induced oscillations. Front Hum Neurosci 9:375. https://doi.org/10.3389/fnhum.2015.00375
Heed T, Röder B (2010) Common anatomical and external coding for hands and feet in tactile attention: evidence from event-related potentials. J Cogn Neurosci 22(1):184–202. https://doi.org/10.1162/jocn.2008.21168%M19199399
Heid C, Mouraux A, Treede RD, Schuh-Hofer S, Rupp A, Baumgärtner U (2020) Early gamma-oscillations as correlate of localized nociceptive processing in primary sensorimotor cortex. J Neurophysiol 123(5):1711–1726. https://doi.org/10.1152/jn.00444.2019
Hsieh J-C, Belfrage M, Stone-Elander S, Hansson P, Ingvar M (1995) Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. PAIN® 63(2):225–236. https://doi.org/10.1016/0304-3959(95)00048-W
Hsieh J-C, Hannerz J, Ingvar M (1996) Right-lateralised central processing for pain of nitroglycer-induced cluster headache. Pain 67(1):59–68. https://doi.org/10.1016/0304-3959(96)03066-7
Iannetti GD, Hughes NP, Lee MC, Mouraux A (2008) Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 100(2):815–828. https://doi.org/10.1152/jn.00097.2008
Ittyerah M (1993) Hand preferences and hand ability in congenitally blind children. Q J Exp Psychol A 46(1):35–50. https://doi.org/10.1080/14640749308401066
Ittyerah M (2013) Hand preference and hand ability: Evidence from studies in haptic cognition (Vol 5). John Benjamins Publishing, Amsterdam
Ittyerah M (2017) Emerging trends in the multimodal nature of cognition: touch and handedness. Front Psychol 8:844. https://doi.org/10.3389/fpsyg.2017.00844
Jensen R, Rasmussen BK, Pedersen B, Lous I, Olesen J (1992) Cephalic muscle tenderness and pressure pain threshold in a general population. Pain 48(2):197–203. https://doi.org/10.1016/0304-3959(92)90059-k
Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377(6545):155–158. https://doi.org/10.1038/377155a0
Karolis VR, Corbetta M, Thiebaut de Schotten M (2019) The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain. Nat Commun 10(1):1417. https://doi.org/10.1038/s41467-019-09344-1
Kinsbourne, M. (1987). Mechanisms of Unilateral Neglect. In M. Jeannerod (Ed.), Advances in Psychology (Vol. 45, pp. 69–86): North-Holland.
Klöppel S, van Eimeren T, Glauche V, Vongerichten A, Münchau A, Frackowiak RS, Siebner HR (2007) The effect of handedness on cortical motor activation during simple bilateral movements. Neuroimage 34(1):274–280. https://doi.org/10.1016/j.neuroimage.2006.08.038
Ladouceur A, Rustamov N, Dubois JD, Tessier J, Lehmann A, Descarreaux M, Piche M (2018) Inhibition of pain and pain-related brain activity by heterotopic noxious counter-stimulation and selective attention in chronic non-specific low back pain. Neuroscience 387:201–213. https://doi.org/10.1016/j.neuroscience.2017.09.054
Landau SM, D’Esposito M (2006) Sequence learning in pianists and nonpianists: an fMRI study of motor expertise. Cogn Affect Behav Neurosci 6(3):246–259. https://doi.org/10.3758/cabn.6.3.246
Lepore F, Lassonde M, Veillette N, Guillemot JP (1997) Unilateral and bilateral temperature comparisons in acallosal and split-brain subjects. Neuropsychologia 35(9):1225–1231. https://doi.org/10.1016/s0028-3932(97)00045-6
Long DA (1994) Hand differences and reported intensity of nociceptive stimuli. Percept Mot Skills 79(1 Pt 2):411–417. https://doi.org/10.2466/pms.1994.79.1.411
Lugo M, Istúriz G, Lara C, García N, Eblen-Zaijur A (2002) Sensory lateralization in pain subjective perception for noxious heat stimulus. Somatosens Mot Res 19(3):207–212. https://doi.org/10.1080/0899022021000009125
Mangin JF, Rivière D, Cachia A, Duchesnay E, Cointepas Y, Papadopoulos-Orfanos D, Régis J (2004) Object-based morphometry of the cerebral cortex. IEEE Trans Med Imaging 23(8):968–982. https://doi.org/10.1109/tmi.2004.831204
Manning L, Thomas-Antérion C (2011) Marc Dax and the discovery of the lateralisation of language in the left cerebral hemisphere. Rev Neurol (paris) 167(12):868–872. https://doi.org/10.1016/j.neurol.2010.10.017
Mazoyer B, Zago L, Jobard G, Crivello F, Joliot M, Perchey G, Tzourio-Mazoyer N (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS ONE 9(6):e101165. https://doi.org/10.1371/journal.pone.0101165
McIntosh AR (2004) Contexts and catalysts: a resolution of the localization and integration of function in the brain. Neuroinformatics 2(2):175–182. https://doi.org/10.1385/ni:2:2:175
McManus IC (1985) Handedness, language dominance and aphasia: a genetic model. Psychol Med Monogr Suppl 8:1–40
Meh D, Denislic M (1994) Quantitative assessment of thermal and pain sensitivity. J Neurol Sci 127(2):164–169. https://doi.org/10.1016/0022-510x(94)90069-8
Melynyte S, Pipinis E, Genyte V, Voicikas A, Rihs T, Griskova-Bulanova I (2018) 40 Hz auditory steady-state response: the impact of handedness and gender. Brain Topogr 31(3):419–429. https://doi.org/10.1007/s10548-017-0611-x
Mesulam M-M (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10(4):309–325. https://doi.org/10.1002/ana.410100402
Millar S, Ai-Attar Z (2003) How do people remember spatial information from tactile maps? Br J vis Impair 21(2):64–72. https://doi.org/10.1177/026461960302100205
Millar S, Al-Attar Z (2003) Spatial reference and scanning with the left and right hand. Perception 32(12):1499–1511. https://doi.org/10.1068/p3424
Mouraux A, Iannetti GD (2008) Across-trial averaging of event-related EEG responses and beyond. Magn Reson Imaging 26(7):1041–1054. https://doi.org/10.1016/j.mri.2008.01.011
Murray FS, Safferstone JF (1970) Pain threshold and tolerance of right and left hands. J Comp Physiol Psychol 71(1):83–86. https://doi.org/10.1037/h0028963
Nativ A, Frank J, Allard F (1989) The effect of handedness on spinal and supra-spinal reflex excitability. Electroencephalogr Clin Neurophysiol 72(2):157–164. https://doi.org/10.1016/0013-4694(89)90177-6
Neubauer S, Gunz P, Scott NA, Hublin JJ, Mitteroecker P (2020) Evolution of brain lateralization: A shared hominid pattern of endocranial asymmetry is much more variable in humans than in great apes. Sci Adv. https://doi.org/10.1126/sciadv.aax9935
Neugebauer V, Mazzitelli M, Cragg B, Ji G, Navratilova E, Porreca F (2020) Amygdala, neuropeptides, and chronic pain-related affective behaviors. Neuropharmacology 170:108052. https://doi.org/10.1016/j.neuropharm.2020.108052
Neziri AY, Andersen OK, Petersen-Felix S, Radanov B, Dickenson AH, Scaramozzino P, Curatolo M (2010) The nociceptive withdrawal reflex: normative values of thresholds and reflex receptive fields. Eur J Pain 14(2):134–141. https://doi.org/10.1016/j.ejpain.2009.04.010
Nicholls ME, Chapman HL, Loetscher T, Grimshaw GM (2010) The relationship between hand preference, hand performance, and general cognitive ability. J Int Neuropsychol Soc 16(4):585–592. https://doi.org/10.1017/s1355617710000184
Northon S, Rustamov N, Piche M (2019) Cortical integration of bilateral nociceptive signals: when more is less. Pain 160(3):724–733. https://doi.org/10.1097/j.pain.0000000000001451
Northon S, Deldar Z, Piché M (2021) Cortical interaction of bilateral inputs is similar for noxious and innocuous stimuli but leads to different perceptual effects. Exp Brain Res. https://doi.org/10.1007/s00221-021-06175-9
Ocklenburg S, Beste C, Güntürkün O (2013) Handedness: a neurogenetic shift of perspective. Neurosci Biobehav Rev 37(10 Pt 2):2788–2793. https://doi.org/10.1016/j.neubiorev.2013.09.014
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113
Otto MW, Dougher MJ, Yeo RA (1989) Depression, pain, and hemispheric activation. J Nerv Ment Dis 177(4):210–218. https://doi.org/10.1097/00005053-198904000-00004
Palomaki KJ, Tiitinen H, Makinen V, May PJ, Alku P (2005) Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques. Brain Res Cogn Brain Res 24(3):364–379. https://doi.org/10.1016/j.cogbrainres.2005.02.013
Pantev C, Lutkenhoner B, Hoke M, Lehnertz K (1986) Comparison between simultaneously recorded auditory-evoked magnetic fields and potentials elicited by ipsilateral, contralateral and binaural tone burst stimulation. Audiology 25(1):54–61. https://doi.org/10.3109/00206098609078369
Pauli P, Wiedemann G, Nickola M (1999) Pain sensitivity, cerebral laterality, and negative affect. Pain 80(1–2):359–364. https://doi.org/10.1016/s0304-3959(98)00231-0
Petersen KL, Brennum J, Olesen J (1992) Evaluation of pericranial myofascial nociception by pressure algometry. Reproducibility and factors of variation. Cephalalgia 12(1):33–37. https://doi.org/10.1046/j.1468-2982.1992.1201033.x
Petit L, Zago L, Mellet E, Jobard G, Crivello F, Joliot M, Tzourio-Mazoyer N (2015) Strong rightward lateralization of the dorsal attentional network in left-handers with right sighting-eye: An evolutionary advantage. Hum Brain Mapp 36(3):1151–1164. https://doi.org/10.1002/hbm.22693
Plaisier MA, Bergmann Tiest WM, Kappers AM (2008) Haptic pop-out in a hand sweep. Acta Psychol (amst) 128(2):368–377. https://doi.org/10.1016/j.actpsy.2008.03.011
Plaisier MA, Tiest WM, Kappers AM (2010) Grabbing subitizing with both hands: bimanual number processing. Exp Brain Res 202(2):507–512. https://doi.org/10.1007/s00221-009-2146-1
Ploner M, Sorg C, Gross J (2017) Brain rhythms of pain. Trends Cogn Sci 21(2):100–110. https://doi.org/10.1016/j.tics.2016.12.001
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. https://doi.org/10.1016/j.neuroimage.2015.01.034
Pud D, Golan Y, Pesta R (2009) Hand dominancy–a feature affecting sensitivity to pain. Neurosci Lett 467(3):237–240. https://doi.org/10.1016/j.neulet.2009.10.048
Reite M, Zimmerman JT, Zimmerman JE (1981) Magnetic auditory evoked fields: interhemispheric asymmetry. Electroencephalogr Clin Neurophysiol 51(4):388–392. https://doi.org/10.1016/0013-4694(81)90102-4
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc Biol Sci 271(Suppl 6):S420-422. https://doi.org/10.1098/rsbl.2004.0200
Rustamov N, Northon S, Tessier J, Leblond H, Piche M (2019) Integration of bilateral nociceptive inputs tunes spinal and cerebral responses. Sci Rep 9(1):7143. https://doi.org/10.1038/s41598-019-43567-y
Salminen NH, Tiitinen H, Miettinen I, Alku P, May PJ (2010) Asymmetrical representation of auditory space in human cortex. Brain Res 1306:93–99. https://doi.org/10.1016/j.brainres.2009.09.095
Sandrini G, Serrao M, Rossi P, Romaniello A, Cruccu G, Willer JC (2005) The lower limb flexion reflex in humans. Prog Neurobiol 77(6):353–395. https://doi.org/10.1016/j.pneurobio.2005.11.003
Sarlani E, Farooq N, Greenspan JD (2003) Gender and laterality differences in thermosensation throughout the perceptible range. Pain 106(1–2):9–18. https://doi.org/10.1016/s0304-3959(03)00211-2
Schlereth T, Baumgärtner U, Magerl W, Stoeter P, Treede RD (2003) Left-hemisphere dominance in early nociceptive processing in the human parasylvian cortex. Neuroimage 20(1):441–454. https://doi.org/10.1016/s1053-8119(03)00345-8
Serrien DJ, Brown P (2002) The functional role of interhemispheric synchronization in the control of bimanual timing tasks. Exp Brain Res 147(2):268–272. https://doi.org/10.1007/s00221-002-1253-z
Serrien DJ, Ivry RB, Swinnen SP (2006) Dynamics of hemispheric specialization and integration in the context of motor control. Nat Rev Neurosci 7(2):160–166. https://doi.org/10.1038/nrn1849
Somers M, Aukes MF, Ophoff RA, Boks MP, Fleer W, de Visser KC, Sommer IE (2015) On the relationship between degree of hand-preference and degree of language lateralization. Brain Lang 144:10–15. https://doi.org/10.1016/j.bandl.2015.03.006
Soto-Faraco S, Ronald A, Spence C (2004) Tactile selective attention and body posture: Assessing the multisensory contributions of vision and proprioception. Percept Psychophys 66(7):1077–1094. https://doi.org/10.3758/BF03196837
Souza VH, Baffa O, Garcia MAC (2018) Lateralized asymmetries in distribution of muscular evoked responses: An evidence of specialized motor control over an intrinsic hand muscle. Brain Res 1684:60–66. https://doi.org/10.1016/j.brainres.2018.01.031
Spernal J, Krieg JC, Lautenbacher S (2003) Pain thresholds as a putative functional test for cerebral laterality in major depressive disorder and panic disorder. Neuropsychobiology 48(3):146–151. https://doi.org/10.1159/000073632
Sperry RW (1974) In Neurosciences third study program. MIT Press, Cambridge, Massachusetts 3:5–19
Stein BE, Price DD, Gazzaniga MS (1989) Pain perception in a man with total corpus callosum transection. Pain 38(1):51–56. https://doi.org/10.1016/0304-3959(89)90072-9
Sun ZY, Klöppel S, Rivière D, Perrot M, Frackowiak R, Siebner H, Mangin JF (2012) The effect of handedness on the shape of the central sulcus. Neuroimage 60(1):332–339. https://doi.org/10.1016/j.neuroimage.2011.12.050
Symonds LL, Gordon NS, Bixby JC, Mande MM (2006) Right-lateralized pain processing in the human cortex: an FMRI study. J Neurophysiol 95(6):3823–3830. https://doi.org/10.1152/jn.01162.2005
Szczepanski SM, Knight RT (2014) Insights into human behavior from lesions to the prefrontal cortex. Neuron 83(5):1002–1018. https://doi.org/10.1016/j.neuron.2014.08.011
Taylor DJ, McGillis SL, Greenspan JD (1993) Body site variation of heat pain sensitivity. Somatosens Mot Res 10(4):455–465. https://doi.org/10.3109/08990229309028850
Tervaniemi M, Hugdahl K (2003) Lateralization of auditory-cortex functions. Brain Res Brain Res Rev 43(3):231–246. https://doi.org/10.1016/j.brainresrev.2003.08.004
Thilmann AF, Schwarz M, Töpper R, Fellows SJ, Noth J (1991) Different mechanisms underlie the long-latency stretch reflex response of active human muscle at different joints. J Physiol 444(1):631–643. https://doi.org/10.1113/jphysiol.1991.sp018898
Tiemann L, Schulz E, Gross J, Ploner M (2010) Gamma oscillations as a neuronal correlate of the attentional effects of pain. Pain 150(2):302–308. https://doi.org/10.1016/j.pain.2010.05.014
Tiemann L, May ES, Postorino M, Schulz E, Nickel MM, Bingel U, Ploner M (2015) Differential neurophysiological correlates of bottom-up and top-down modulations of pain. Pain 156(2):289–296. https://doi.org/10.1097/01.j.pain.0000460309.94442.44
Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4(1):37–48. https://doi.org/10.1038/nrn1009
Tononi G, Edelman GM, Sporns O (1998) Complexity and coherency: integrating information in the brain. Trends Cogn Sci 2(12):474–484. https://doi.org/10.1016/s1364-6613(98)01259-5
Trumbower RD, Finley JM, Shemmell JB, Honeycutt CF, Perreault EJ (2013) Bilateral impairments in task-dependent modulation of the long-latency stretch reflex following stroke. Clin Neurophysiol 124(7):1373–1380. https://doi.org/10.1016/j.clinph.2013.01.013
Ungan P, Yagcioglu S, Goksoy C (2001) Differences between the N1 waves of the responses to interaural time and intensity disparities: scalp topography and dipole sources. Clin Neurophysiol 112(3):485–498. https://doi.org/10.1016/s1388-2457(00)00550-2
Vaid J, Bellugi U, Poizner H (1989) Hand dominance for signing: clues to brain lateralization of language. Neuropsychologia 27(7):949–960. https://doi.org/10.1016/0028-3932(89)90070-5
Vierck CJ Jr, Staud R, Price DD, Cannon RL, Mauderli AP, Martin AD (2001) The effect of maximal exercise on temporal summation of second pain (windup) in patients with fibromyalgia syndrome. J Pain 2(6):334–344. https://doi.org/10.1054/jpai.2001.25533
White LE, Lucas G, Richards A, Purves D (1994) Cerebral asymmetry and handedness. Nature 368(6468):197–198. https://doi.org/10.1038/368197a0
Whitehouse AJ, Bishop DV (2009) Hemispheric division of function is the result of independent probabilistic biases. Neuropsychologia 47(8–9):1938–1943. https://doi.org/10.1016/j.neuropsychologia.2009.03.005
Willems RM, Van der Haegen L, Fisher SE, Francks C (2014) On the other hand: including left-handers in cognitive neuroscience and neurogenetics. Nat Rev Neurosci 15(3):193–201. https://doi.org/10.1038/nrn3679
Willer JC (1977) Comparative study of perceived pain and nociceptive flexion reflex in man. Pain 3(1):69–80. https://doi.org/10.1016/0304-3959(77)90036-7
Woytowicz EJ, Westlake KP, Whitall J, Sainburg RL (2018) Handedness results from complementary hemispheric dominance, not global hemispheric dominance: evidence from mechanically coupled bilateral movements. J Neurophysiol 120(2):729–740. https://doi.org/10.1152/jn.00878.2017
Youell PD, Wise RG, Bentley DE, Dickinson MR, King TA, Tracey I, Jones AK (2004) Lateralisation of nociceptive processing in the human brain: a functional magnetic resonance imaging study. Neuroimage 23(3):1068–1077. https://doi.org/10.1016/j.neuroimage.2004.07.004
Funding
This work was supported by a grant from the Natural Science and Engineering Research Council of Canada (#06659) and the Canadian Foundation for Innovation (#33731). The contribution of Stéphane Northon was supported by the Fonds de Recherche du Québec en Nature et Technologie. The contribution of Zoha Deldar was supported by the Department of Anatomy of the Université du Québec à Trois-Rivières and the Centre de recherche en Neuropsychologie et Cognition. The contribution of Mathieu Piché was supported by the Fonds de Recherche du Québec en Santé. Figure 1 was created with BioRender.com.
Author information
Authors and Affiliations
Contributions
All authors contributed significantly to this study and has read the final version of the manuscript. Stéphane Northon and Zoha Deldar contributed equally to this work. S.N. contributed to data collection and analyses and manuscript writing. Z.D contributed to data collection and wrote the first version of the manuscript. M.P. contributed to study design, data collection, analyses and interpretation, wrote the final version of the manuscript and obtained funding.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests and no relationship that may lead to any conflict of interest.
Ethical approval
All experimental procedures conformed to the standards set by the latest revision of the Declaration of Helsinki and were approved by the Research Ethics Board of the Université du Québec à Trois-Rivières.
Consent to participate
All participants received written informed consent, acknowledged their right to withdraw from the experiment without prejudice, and received a compensation of $25 for their travel expenses, time, and commitment.
Consent for publication
Not applicable.
Additional information
Handling Editor: Micah M. Murray.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Northon, S., Deldar, Z. & Piché, M. Spinal and Cerebral Integration of Noxious Inputs in Left-handed Individuals. Brain Topogr 34, 568–586 (2021). https://doi.org/10.1007/s10548-021-00864-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-021-00864-y