Abstract
Oscillatory activity in the beta (β)-frequency band (13–35 Hz) can be recorded over the sensorimotor cortex in humans. It is coherent with electromyographic activity (EMG) during tonic contraction, but whether the cortical β-oscillations are primarily motor or sensorimotor in function remains unclear. We tested the hypothesis that cortical β-activity is associated with an up-regulation of sensory inputs that may be relevant to the organization of the motor response. We recorded cortical somatosensory potentials (SEPs) elicited by electrical stimuli to the median nerve at the wrist triggered by increases of electroencephalographic (EEG) β-activity in the contralateral fronto-central EEG and compared these to SEPs presented at random intervals. The involvement of motor cortex in the triggering EEG activity was confirmed by a simultaneous elevation of cortico-spinal synchrony in the β-band. The negative cortical evoked potential peaking at 20 ms and the positive evoked potential peaking at 30 ms after median nerve shocks were increased in size when elicited after phasic increases in β-activity. The functional coupling of sensory and motor cortices in the β-band was confirmed in recordings of electrocorticographic activity in two patients with chronic pain syndromes, suggesting a means by which β-activity may simultaneously influence cortical sensory processing, motor output and promote sensory-motor interaction.
Similar content being viewed by others
References
Allison T, McCarthy G, Wood CC, Jones SJ (1991) Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. Brain 114:2465–503
Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501:225–241
Baker SN, Kilner JM, Pinches EM, Lemon RN (1999) The role of synchrony and oscillations in the motor output. Exp Brain Res 128:109–117
Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci USA 101:9849–9854
Brown P, Salenius S, Rothwell JC, Hari R (1998) The cortical correlate of the Piper rhythm in man. J Neurophysiol 80:2911–2917
Brown P, Farmer S F, Halliday DM, Marsden J, Rosenberg JR (1999) Coherent cortical and muscle discharge in cortical myoclonus. Brain 122:461–472
Cakmur R, Towle VL, Mullan JF, Suarez D, Spire JP (1997) Intra-operative localization of sensorimotor cortex by cortical somatosensory evoked potentials:from analysis of waveforms to dipole source modeling. Acta Neurochir (Wien) 139:1117–1125
Cassim F, Monaca C, Szurhaj W, Bourriez JL, Defebvre L, Derambure P et al (2001) Does post-movement beta synchronization reflect an idling motor cortex? Neuroreport 12:3859–3863
Conway BA, Halliday DM, Farmer SF, Shahani U, Maas P, Weir AI, Rosenberg JR (1995) Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489:917–924
Day BL, Riescher H, Struppler A, Rothwell JC, Marsden CD (1991) Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man. J Physiol 433:41–57
Donoghue JP, Sanes JN, Hatsopoulos NG, Gaal G (1998) Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J Neurophysiol 79:159–173
Gilbertson T, Lalo E, Doyle L, Di Lazzaro V, Cioni B, Brown P (2005) Existing motor state is favored at the expense of new movement during 13–35 Hz oscillatory synchrony in the human corticospinal system. J Neurosci 25:7771–7779
Gross J, Tass PA, Salenius S, Hari R, Freund HJ, Schnitzler A (2000) Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography. J Physiol 527:623–631
Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, Farmer SF (1995) A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64:237–278
Hoshiyama M, Kakigi R (2001) Correspondence between short-latency somatosensory evoked brain potentials and cortical magnetic fields flowing median nerve stimulation. Brain Res 908:140–148
Insola A, Le Pera D, Restuccia D, Mazzone P, Valeriani M (2004) Reduction in amplitude of the subcortical low- and high-frequency somatosensory evoked potentials during voluntary movement: an intracerebral recording study. Clin Neurophysiol 15:104–111
Kilner JM, Baker SN, Salenius S, Jousmaki V, Hari R, Lemon RN (1999) Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol 516:559–570
Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94:1904–1911
Macefield VG, Rothwell JC, Day BL (1996) The contribution of transcortical pathways to long-latency stretch and tactile reflexes in human hand muscles. Exp Brain Res 108:147–154
Marsden CD, Merton PA, Morton HB (1976) Stretch reflex and servo action in a variety of human muscles. J Physiol 259:531–560
Marsden CD, Merton PA, Morton HB, Adam J (1977a) The effect of lesions of the sensorimotor cortex and the capsular pathways on servo responses from the human long thumb flexor. Brain 100:503–526
Marsden CD, Merton PA, Morton HB, Adam J (1977b) The effect of posterior column lesions on servo responses from the human long thumb flexor. Brain 100:185–200
Massimini M, Rosanova M, Mariotti M (2003) EEG slow (approximately 1 Hz) waves are associated with nonstationarity of thalamo-cortical sensory processing in the slee** human. J Neurophysiol 89:1205–1213
Miles TS, Flavel SC, Nordstrom MA (2004) Stretch reflexes in the human masticatory muscles: a brief review and a new functional role. Hum Mov Sci 23:337–349
Murthy VN, Fetz EE (1992) Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 89:5670–5674
Murthy VN, Fetz EE (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76:3968–3982
Myers LJ, Lowery M, O’Malley M, Vaughan C L, Heneghan C, St Clair Gibson A, Harley YX, Sreenivasan R (2003) Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis. J Neurosci Methods 124:157–165
Palmer E, Ashby P (1992) Evidence that a long latency stretch reflex in humans is transcortical. J Physiol 449:429–440
Porter R, Lemon RN (1993) Corticospinal function and voluntary movement. Clarendon Press, Oxford
Rossini PM, Babiloni C, Babiloni F, Ambrosini A, Onorati P, Carducci F, Urbano A (1999) “Gating” of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study. Brain Res 843:161–170
Salenius S, Portin K, Kajola M, Salmelin R, Hari R (1997) Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 77:3401–3405
Sanes JN, Donoghue JP (1993) Oscillations in local field potentials of the primate motor cortex during voluntary movement. Proc Natl Acad Sci USA 90:4470–4474
Schnitzler A, Salenius S, Salmelin R, Jousmaki V, Hari R (1997) Involvement of primary motor cortex in motor imagery: a neuromagnetic study. Neuroimage 6:201–208
Schoffelen JM, Oostenveld R, Fries P (2005) Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308:111–113
Stancak A Jr, Pfurtscheller G (1996) Event-related desynchronisation of central beta-rhythms during brisk and slow self-paced finger movements of dominant and nondominant hand. Brain Res Cogn Brain Res 4:171–183
Valeriani M, Restuccia D, Barba C, Tonali P, Mauguiere F (2000) Central scalp projection of the N30 SEP source activity after median nerve stimulation. Muscle Nerve 23:353–360
Wallace CJ, Miles TS (1998) Movements modulate the reflex responses of human flexor pollicis longus to stretch. Exp Brain Res 118:105–110
Wallace CJ, Miles TS (2001) Cortical excitability is not depressed in movement-modulated stretch response of human thumb flexor. Exp Brain Res 139:448–453
Wasaka T, Hoshiyama M, Nakata H, NishihiraY, Kakigi R (2003) Gating of somatosensory evoked magnetic fields during the preparatory period of self-initiated finger movement. Neuroimage 20:1830–1838
Acknowledgments
This work was supported by the Association France-Parkinson (E.L.), Amulree Trust (T.G.) and the Medical Research Council of Great Britain (L.D. and P.B.).
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article can be found at http://dx.doi.org/10.1007/s00221-006-0828-5
Rights and permissions
About this article
Cite this article
Lalo, E., Gilbertson, T., Doyle, L. et al. Phasic increases in cortical beta activity are associated with alterations in sensory processing in the human . Exp Brain Res 177, 137–145 (2007). https://doi.org/10.1007/s00221-006-0655-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-006-0655-8