The human dorsal premotor cortex facilitates the excitability of ipsilateral primary motor cortex via a short latency cortico-cortical route

Human Brain Mapping

Volumn 33, Issue 2, 2012, Pages 419-430

  Groppa, Sergiu ^a   Schlaak, Boris H ^a   Münchau, Alexander ^b   Werner Petroll, Nicole ^a   Dünnweber, Janin ^a   Bäumer, Tobias ^b   van Nuenen, Bart F L ^a,c   Siebner, Hartwig R ^a,d,e  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d HVIDOVRE HOSPITAL   (Denmark)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Connectivity; Dorsal premotor cortex; I waves; Motor cortex; Transcranial magnetic stimulation

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; EXCITATION; HEMISPHERE; HUMAN; LATENT PERIOD; MALE; NORMAL HUMAN; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TRANSCRANIAL MAGNETIC STIMULATION;

EVOKED POTENTIALS, MOTOR; HAND; HUMANS; MALE; MOTOR CORTEX; MUSCLE, SKELETAL; NEURAL PATHWAYS; PREFRONTAL CORTEX; REACTION TIME; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84855972327     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21221     Document Type: Article

References (43)

1. Amassian VE, Stewart M, Quirk GJ, Rosenthal JL (1987): Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 20: 74-93.
2. Barker AT, Jalinous R, Freeston IL (1985): Non-invasive magnetic stimulation of human motor cortex. Lancet 1: 1106-1107.
3. Baumer T, Bock F, Koch G, Lange R, Rothwell JC, Siebner HR, Munchau A (2006): Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. J Physiol 572 (Part 3): 857-868.
4. Baumer T, Schippling S, Kroeger J, Zittel S, Koch G, Thomalla G, Rothwell JC, Siebner HR, Orth M, Munchau A (2009): Inhibitory and facilitatory connectivity from ventral premotor to primary motor cortex in healthy humans at rest: A bifocal TMS study. Clin Neurophysiol 120: 1724-1731.
5. Boorman ED, O'Shea J, Sebastian C, Rushworth MFS, Johansen-Berg H (2007): Individual differences in white-matter microstructure reflect variation in functional connectivity during choice. Curr Biol 17: 1426-1431.
6. Burke D, Hicks R, Gandevia SC, Stephen J, Woodforth I, Crawford M (1993): Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol 470: 383-393.
7. Cerri G, Shimazu H, Maier MA, Lemon RN (2003): Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. J Neurophysiol 90: 832-842.
8. Civardi C, Cantello R, Asselman P, Rothwell JC (2001): Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14: 1444-1453.
9. Davare M, Lemon RN, Olivier E (2008): Selective modulations of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J Physiol 586:2735-2742.
10. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999a): Direct recordings of descending volleys after transcranial magnetic and electric motor cortex stimulation in conscious humans. Electroencephalogr Clin Neurophysiol Suppl 51: 120-126.
11. Di Lazzaro V, Rothwell JC, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P (1999b): Intracortical origin of the short latency facilitation produced by pairs of threshold magnetic stimuli applied to human motor cortex. Exp Brain Res 129: 494-499.
12. Di Lazzaro V, Profice P, Pilato F, Dileone M, Oliviero A, Ziemann U (2010): The effects of motor cortex rTMS on corticospinal descending activity. Clin Neurophysiol 121: 464-473.
13. Dum RP, Strick PL (1991): The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11: 667-689.
14. Dum RP, Strick PL (2002): Motor areas in the frontal lobe of the primate. Physiol Behav 77: 677-682.
15. Dum RP, Strick PL (2005): Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci 25: 1375-1386.
16. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992): Interhemispheric inhibition of the human motor cortex. J Physiol 453: 525-546.
17. Hallett M (2000): Transcranial magnetic stimulation and the human brain. Nature 406: 147-150.
18. He SQ, Dum RP, Strick PL (1993): Topographic organization of corticospinal projections from the frontal lobe: Motor areas on the lateral surface of the hemisphere. J Neurosci 13: 952-980.
19. He SQ, Dum RP, Strick PL (1995): Topographic organization of corticospinal projections from the frontal lobe: Motor areas on the medial surface of the hemisphere. J Neurosci 15 (5 Part 1): 3284-3306.
20. Kermadi I, Liu Y, Tempini A, Calciati E, Rouiller EM (1998): Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens Motor Res 15: 287-308.
21. Koch G, Franca M, Del Olmo MF, Cheeran B, Milton R, Alvarez Sauco M, Rothwell JC (2006): Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J Neurosci 26: 7452-7459.
22. Koch G, Fernandez Del Olmo M, Cheeran B, Ruge D, Schippling S, Caltagirone C, Rothwell JC (2007a): Focal stimulation of the posterior parietal cortex increases the excitability of the ipsilateral motor cortex. J Neurosci 27: 6815-6822.
23. Koch G, Franca M, Mochizuki H, Marconi B, Caltagirone C, Rothwell JC (2007b): Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J Physiology 578: 551-562.
24. Lemon RN (2008): Descending pathways in motor control. Annu Rev Neurosci 31: 195-218.
25. Luppino G, Matelli M, Camarda RM, Rizzolatti G (1993): Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Compar Neurol 338: 114-140.
26. Martino AM, Strick PL (1987): Corticospinal projections originate from the arcuate premotor area. Brain Res 404: 307-312.
27. Matelli M, Camarda R, Glickstein M, Rizzolatti G (1984): Interconnections within the postarcuate cortex (area 6) of the macaque monkey. Brain Res 310: 388-392.
28. Mochizuki H, Huang YZ, Rothwell JC (2004): Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. J Physiol 561 (Part 1): 331-338.
29. O'Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MF (2007): Functional specificity of human premotor-motor cortical interactions during action selection. Eur J Neurosci 26: 2085-2095.
30. Patton HD, Amassian VE (1954): Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J Neurophysiol 17: 345-363.
31. Petrides M (1985): Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 23: 601-614.
32. Picard N, Strick PL (2001): Imaging the premotor areas. Curr Opin Neurobiol 11: 663-672.
33. Prabhu G, Shimazu H, Cerri G, Brochier T, Spinks RL, Maier MA, Lemon RN (2009): Modulation of primary motor cortex outputs from ventral premotor cortex during visually-guided grasp in the macaque monkey. J Physiology 587:1057-1069.
34. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH (1994): Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91: 79-92.
35. Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997): Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp Brain Res 113: 24-32.
36. Schluter ND, Rushworth MF, Passingham RE, Mills KR (1998): Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. Brain 121 (Part 5): 785-799.
37. Schmidlin E, Brochier T, Maier MA, Kirkwood PA, Lemon RN (2008): Pronounced reduction of digit motor responses evoked from macaque ventral premotor cortex after reversible inactivation of the primary motor cortex hand area. J Neurosci 28: 5772-5783.
38. Shimazu H, Maier MA, Cerri G, Kirkwood PA, Lemon RN (2004): Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J Neurosci 24: 1200-1211.
39. Tokimura H, Ridding MC, Tokimura Y, Amassian VE, Rothwell JC (1996): Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. Electroencephalogr Clin Neurophysiol 101: 263-272.
40. Tokuno H, Nambu A (2000): Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: An electrophysiological study in the macaque monkey. Cereb Cortex 10: 58-68.
41. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997): Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120: 141-157.
42. Ziemann U, Rothwell JC (2000): I-waves in motor cortex. J Clin Neurophysiol 17: 397-405.
43. Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W (1998): Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 511 (Part 1): 181-190.