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Interactions between short latency afferent inhibition and long interval intracortical inhibition

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Abstract

Peripheral nerve stimulation inhibits the motor cortex and the process has been termed afferent inhibition. Short latency afferent inhibition (SAI) at interstimulus intervals (ISI) of ~20 ms likely involves central cholinergic transmission and was found to be altered in Alzheimer’s disease and Parkinson’s disease. Cholinergic and GABAA receptors are involved in mediating SAI. The effects of SAI on other intracortical inhibitory and facilitatory circuits have not been examined. The objective of the present study is to test how SAI interacts with long interval cortical inhibition (LICI), a cortical inhibitory circuit likely mediated by GABAB receptors. We studied 10 healthy volunteers. Surface electromyogram was recorded from the first dorsal interosseous muscle. SAI was elicited by median nerve stimulation at the wrist followed by transcranial magnetic stimulation (TMS) at ISI of N20 somatosensory evoked potential latency + 3 ms. The effects of different test motor-evoked potential (MEP) amplitudes (0.2, 1, and 2 mV) were examined for LICI and SAI. Using paired and triple-pulse paradigms, the interactions between SAI and LICI were investigated. Both LICI and SAI decreased with increasing test MEP amplitude. Afferent stimulation that produced SAI decreased LICI. Thus, the present findings suggest that LICI and SAI have inhibitory interactions.

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References

  • Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C (2001) Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain 124:537–545

    Article  PubMed  CAS  Google Scholar 

  • Aimonetti JM, Nielsen JB (2001) Changes in intracortical excitability induced by stimulation of wrist afferents in man. J Physiol 534:891–902

    Article  PubMed  CAS  Google Scholar 

  • Berardelli A, Rona S, Inghilleri M, Manfredi M (1996) Cortical inhibition in Parkinson’s disease. A study with paired magnetic stimulation. Brain 119:71–77

    Article  PubMed  Google Scholar 

  • Bikmullina R, Kicic D, Carlson S, Nikulin VV (2009) Electrophysiological correlates of short-latency afferent inhibition: a combined EEG and TMS study. Exp Brain Res 194:517–526

    Article  PubMed  Google Scholar 

  • Chen R (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 154:1–10

    Article  PubMed  Google Scholar 

  • Chen R, Corwell B, Hallett M (1999) Modulation of motor cortex excitability by median nerve and digit stimulation. Exp Brain Res 129:77–86

    Article  PubMed  CAS  Google Scholar 

  • Chu J, Wagle-Shukla A, Gunraj C, Lang AE, Chen R (2009) Impaired presynaptic inhibition in the motor cortex in Parkinson disease. Neurology 72:842–849

    Article  PubMed  CAS  Google Scholar 

  • Classen J, Steinfelder B, Liepert J, Stefan K, Celnik P, Cohen LG, Hess A, Kunesch E, Chen R, Benecke R, Hallett M (2000) Cutaneomotor integration in humans is somatotopically organized at various levels of the nervous system and is task dependent. Exp Brain Res 130:48–59

    Article  PubMed  CAS  Google Scholar 

  • Delwaide PJ, Olivier E (1990) Conditioning transcranial cortical stimulation (TCCS) by exteroceptive stimulation in parkinsonian patients. Adv Neurol 53:175–181

    PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 135:455–461

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, Saturno E, Pilato F, Masullo C, Rothwell JC (2002) Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 59:392–397

    PubMed  Google Scholar 

  • Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Ghirlanda S, Ranieri F, Gainotti G, Tonali P (2005a) Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76:1064–1069

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Saturno E, Dileone M, Pilato F, Nardone R, Ranieri F, Musumeci G, Fiorilla T, Tonali P (2005b) Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 564:661–668

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Pilato F, Dileone M, Saturno E, Oliviero A, Marra C, Daniele A, Ranieri F, Gainotti G, Tonali PA (2006) In vivo cholinergic circuit evaluation in frontotemporal and Alzheimer dementias. Neurology 66:1111–1113

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Pilato F, Dileone M, Profice P, Ranieri F, Ricci V, Bria P, Tonali PA, Ziemann U (2007) Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: A TMS study. Clin Neurophysiol 118:2207–2214

    Article  PubMed  CAS  Google Scholar 

  • Fierro B, Brighina F, D’Amelio M, Daniele O, Lupo I, Ragonese P, Palermo A, Savettieri G (2008) Motor intracortical inhibition in PD: L-DOPA modulation of high-frequency rTMS effects. Exp Brain Res 184:521–528

    Article  PubMed  Google Scholar 

  • Kaneko K, Kawai S, Fuchigami Y, Morita H, Ofuji A (1996) The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. Electroencephalogr Clin Neurophysiol 101:478–482

    Article  PubMed  CAS  Google Scholar 

  • McDonnell MN, Thompson PD, Ridding MC (2007) The effect of cutaneous input on intracortical inhibition in focal task-specific dystonia. Mov Disord 22:1286–1292

    Article  PubMed  Google Scholar 

  • Muller-Dahlhaus FJM, Liu Y, Ziemann U (2008) Inhibitory circuits and the nature of their interactions in the human motor cortex a pharmacological TMS study. J Physiol 586:495–514

    PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Oliviero A, Leon AM, Holler I, Vila JF, Siebner HR, Della MG, Di LV, Alvarez JT (2005) Reduced sensorimotor inhibition in the ipsilesional motor cortex in a patient with chronic stroke of the paramedian thalamus. Clin Neurophysiol 116:2592–2598

    Article  PubMed  CAS  Google Scholar 

  • Pierantozzi M, Palmieri MG, Marciani MG, Bernardi G, Giacomini P, Stanzione P (2001) Effect of apomorphine on cortical inhibition in Parkinson’s disease patients: a transcranial magnetic stimulation study. Exp Brain Res 141:52–62

    Article  PubMed  CAS  Google Scholar 

  • Sailer A, Molnar GF, Cunic DI, Chen R (2002) Effects of peripheral sensory input on cortical inhibition in humans. J Physiol (Lond) 544:617–629

    Article  CAS  Google Scholar 

  • Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson’s disease. Brain 126:1883–1894

    Article  PubMed  Google Scholar 

  • Sailer A, Cunic DI, Paradiso GO, Gunraj CA, Wagle-Shukla A, Moro E, Lozano AM, Lang AE, Chen R (2007) Subthalamic deep brain stimulation modulates afferent inhibition in Parkinson’s disease. Neurology 68:356–364

    Article  PubMed  CAS  Google Scholar 

  • Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol (Lond) 530:307–317

    Article  CAS  Google Scholar 

  • Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584

    Article  PubMed  Google Scholar 

  • Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory input from the hand. J Physiol (Lond) 523:503–513

    Article  CAS  Google Scholar 

  • Trompetto C, Buccolieri A, Abbruzzese G (2001) Intracortical inhibitory circuits and sensory input: a study with transcranial magnetic stimulation in humans. Neurosci Lett 297:17–20

    Article  PubMed  CAS  Google Scholar 

  • Werhahn KJ, Fong JKY, Meyer BU, Priori A, Rothwell JC, Day BL, Thompson PD (1994) The effect of magnetic coil orientation on the latency of surface EMG and single motor unit responses in the first dorsal interosseous muscle. Electroencephalogr Clin Neurophysiol 93:138–146

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This study was funded by the Canadian Institutes of Health Research grant No: MOP 62917.

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Authors and Affiliations

  1. Division of Neurology, Department of Medicine, University of Toronto, Toronto, ON, Canada

    Kaviraja Udupa, Zhen Ni & Robert Chen

  2. Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research Institute, University Health Network, MP 13-304, 399 Bathurst Street, Toronto, ON, M5T 2S8, Canada

    Kaviraja Udupa, Zhen Ni & Carolyn Gunraj

  3. Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research Institute, University Health Network, 7MC-411, 399 Bathurst Street, Toronto, ON, M5T 2S8, Canada

    Robert Chen

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  1. Kaviraja Udupa
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  2. Zhen Ni
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  4. Robert Chen
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Correspondence to Robert Chen.

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Udupa, K., Ni, Z., Gunraj, C. et al. Interactions between short latency afferent inhibition and long interval intracortical inhibition. Exp Brain Res 199, 177–183 (2009). https://doi.org/10.1007/s00221-009-1997-9

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  • DOI: https://doi.org/10.1007/s00221-009-1997-9

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