Experimental Brain Research

, 199:177 | Cite as

Interactions between short latency afferent inhibition and long interval intracortical inhibition

  • Kaviraja Udupa
  • Zhen Ni
  • Carolyn Gunraj
  • Robert Chen
Research Article


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.


Transcranial magnetic stimulation Motor cortex Intracortical circuits Short latency afferent inhibition Long interval intracortical inhibition 


  1. Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C (2001) Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain 124:537–545PubMedCrossRefGoogle Scholar
  2. Aimonetti JM, Nielsen JB (2001) Changes in intracortical excitability induced by stimulation of wrist afferents in man. J Physiol 534:891–902PubMedCrossRefGoogle Scholar
  3. Berardelli A, Rona S, Inghilleri M, Manfredi M (1996) Cortical inhibition in Parkinson’s disease. A study with paired magnetic stimulation. Brain 119:71–77PubMedCrossRefGoogle Scholar
  4. 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 194:517–526PubMedCrossRefGoogle Scholar
  5. Chen R (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 154:1–10PubMedCrossRefGoogle Scholar
  6. Chen R, Corwell B, Hallett M (1999) Modulation of motor cortex excitability by median nerve and digit stimulation. Exp Brain Res 129:77–86PubMedCrossRefGoogle Scholar
  7. Chu J, Wagle-Shukla A, Gunraj C, Lang AE, Chen R (2009) Impaired presynaptic inhibition in the motor cortex in Parkinson disease. Neurology 72:842–849PubMedCrossRefGoogle Scholar
  8. 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 130:48–59PubMedCrossRefGoogle Scholar
  9. Delwaide PJ, Olivier E (1990) Conditioning transcranial cortical stimulation (TCCS) by exteroceptive stimulation in parkinsonian patients. Adv Neurol 53:175–181PubMedGoogle Scholar
  10. 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 135:455–461PubMedCrossRefGoogle Scholar
  11. 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 59:392–397PubMedGoogle Scholar
  12. 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 76:1064–1069PubMedCrossRefGoogle Scholar
  13. 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 564:661–668PubMedCrossRefGoogle Scholar
  14. 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 66:1111–1113PubMedCrossRefGoogle Scholar
  15. 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 118:2207–2214PubMedCrossRefGoogle Scholar
  16. 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 184:521–528PubMedCrossRefGoogle Scholar
  17. 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 101:478–482PubMedCrossRefGoogle Scholar
  18. McDonnell MN, Thompson PD, Ridding MC (2007) The effect of cutaneous input on intracortical inhibition in focal task-specific dystonia. Mov Disord 22:1286–1292PubMedCrossRefGoogle Scholar
  19. 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 586:495–514PubMedGoogle Scholar
  20. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  21. 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 116:2592–2598PubMedCrossRefGoogle Scholar
  22. 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 141:52–62PubMedCrossRefGoogle Scholar
  23. Sailer A, Molnar GF, Cunic DI, Chen R (2002) Effects of peripheral sensory input on cortical inhibition in humans. J Physiol (Lond) 544:617–629CrossRefGoogle Scholar
  24. Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson’s disease. Brain 126:1883–1894PubMedCrossRefGoogle Scholar
  25. 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 68:356–364PubMedCrossRefGoogle Scholar
  26. Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol (Lond) 530:307–317CrossRefGoogle Scholar
  27. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584PubMedCrossRefGoogle Scholar
  28. 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) 523:503–513CrossRefGoogle Scholar
  29. Trompetto C, Buccolieri A, Abbruzzese G (2001) Intracortical inhibitory circuits and sensory input: a study with transcranial magnetic stimulation in humans. Neurosci Lett 297:17–20PubMedCrossRefGoogle Scholar
  30. 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 93:138–146PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kaviraja Udupa
    • 1
    • 2
  • Zhen Ni
    • 1
    • 2
  • Carolyn Gunraj
    • 2
  • Robert Chen
    • 1
    • 3
  1. 1.Division of Neurology, Department of MedicineUniversity of TorontoTorontoCanada
  2. 2.Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research InstituteUniversity Health NetworkTorontoCanada
  3. 3.Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research InstituteUniversity Health NetworkTorontoCanada

Personalised recommendations