Neck muscle responses evoked by transcranial magnetic stimulation of the human frontal eye fields

European Journal of Neuroscience

Volumn 33, Issue 11, 2011, Pages 2155-2167

  Goonetilleke, Samanthi C ^a   Gribble, Paul L ^a   Mirsattari, Seyed M ^a   Doherty, Timothy J ^a   Corneil, Brian D ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Electromyography; Eye head gaze shifts; Frontal cortex; Oculomotor

Indexed keywords

ADULT; ARTICLE; ATTENUATION; BRAIN FUNCTION; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; FEMALE; FRONTAL EYE FIELD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; MOTOR CORTEX; MUSCLE CONTRACTION; NECK MUSCLE; NORMAL HUMAN; OCULOMOTOR SYSTEM; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SKELETAL MUSCLE; SPLENIUS CAPITIS; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL MEMORY;

ADULT; ELECTROMYOGRAPHY; FEMALE; HUMANS; MALE; MEMORY; NECK MUSCLES; REACTION TIME; SACCADES; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL FIELDS;

EID: 79958031528     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07711.x     Document Type: Article

References (75)

1. André-Deshays, C., Berthoz, A. & Revel, M. (1988) Eye-head coupling in humans. I. Simultaneous recording of isolated motor units in dorsal neck muscle and horizontal eye movements. Exp. Brain Res., 69, 399-406.
2. André-Deshays, C., Revel, M. & Berthoz, A. (1991) Eye-head coupling in humans. II. Phasic components. Exp. Brain Res., 84, 359-366.
3. Bexander, C.S.M., Mellor, R. & Hodges, P.W. (2005) Effect of gaze direction on neck muscle activity during cervical rotation. Exp. Brain Res., 167, 422-432.
4. Blouin, J.S., Siegmund, G.P., Carpenter, M.G. & Inglis, J.T. (2007) Neural control of superficial and deep neck muscles in humans. J. Neurophysiol., 98, 920-928.
5. Boulanger, M., Bergeron, A. & Guitton, D. (2009) Ipsilateral head and centring eye movements evoked from monkey premotor cortex. Neuroreport, 20, 669-673.
6. Carl, J.R. (1993) Principles and techniques of electro-oculography. In Jacobson, G.P., Newman, C.W. & Kartush, J.M. (Eds), Handbook of Balance Function Testing. Singular Publishing Group, San Diego, CA, pp. 69-82.
7. Chen, L.L.T. (2006) Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control. J. Neurophysiol., 95, 3528-3542.
8. Corneil, B.D., Olivier, E., Richmond, F.J.R., Loeb, G.E. & Munoz, D.P. (2001) Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. J. Neurophysiol., 86, 1729-1749.
9. Corneil, B.D., Olivier, E. & Munoz, D.P. (2002) Neck muscle responses to stimulation of monkey superior colliculus. II. Gaze shift initiation and volitional head movements. J. Neurophysiol., 88, 2000-2018.
10. Corneil, B.D., Olivier, E. & Munoz, D.P. (2004) Visual responses on neck muscles reveal selective gating that prevents express saccades. Neuron, 42, 831-841.
11. Corneil, B.D., Munoz, D.P. & Olivier, E. (2007) Priming of head premotor circuits during oculomotor preparation. J. Neurophysiol., 97, 701-714.
12. Corneil, B.D., Munoz, D.P., Chapman, B.B., Admans, T. & Cushing, S.L. (2008) Neuromuscular consequences of reflexive covert orienting. Nat. Neurosci., 11, 13-15.
13. Corneil, B.D., Elsley, J.K., Nagy, B. & Cushing, S.L. (2010) Motor output evoked by subsaccadic stimulation of primate frontal eye fields. Proc. Natl Acad. Sci. USA, 107, 6070-6075.
14. Dorris, M.C., Paré, M. & Munoz, D.P. (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J. Neurosci., 17, 8566-8579.
15. Dum, R.P. & Strick, P.L. (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. Ekstrom, L.B., Roelfsema, P.R., Arsenault, J.T., Bonmassar, G. & Vanduffel, W. (2008) Bottom-up dependent gating of frontal signals in early visual cortex. Science, 321, 414-417.
17. Elsley, J.K., Nagy, B., Cushing, S.L. & Corneil, B.D. (2007) Widespread presaccadic recruitment of neck muscles by stimulation of the primate frontal eye fields. J. Neurophysiol., 98, 1333-1354.
18. Fries, W. (1984) Cortical projections to the superior colliculus in the macaque monkey - a retrograde study using horseradish-peroxidase. J. Comp. Neurol., 230, 55-76.
19. Galiana, H.L. & Guitton, D. (1992) Central organization and modeling of eye-head coordination during orienting gaze shifts. Ann. NY Acad. Sci., 656, 452-471.
20. Gandhi, N.J. & Sparks, D.L. (2007) Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region. J. Neurophysiol., 98, 360-373.
21. Ghosh, S. & Gattera, R. (1995) A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. Somatosens. Mot. Res., 12, 359-378.
22. Godschalk, M., Lemon, R.N., Kuypers, H. & Ronday, H.K. (1984) Cortical afferents and efferents of monkey postarcuate area - an anatomical and electrophysiological study. Exp. Brain Res., 56, 410-424.
23. Goonetilleke, S.C., Gribble, P.L., Mirsattari, S.M., Doherty, T.J. & Corneil, B.D. (2009) Studying the excitability of the human frontal eye fields using transcranial magnetic stimulation and electromyography. Soc. Neurosci., Abstract, 405, 1.
24. Goonetilleke, S.C., Doherty, T.J. & Corneil, B.D. (2010) A within trial measure of the stop signal reaction time in a head-unrestrained oculomotor countermanding task. J. Neurophysiol., 104, 3677-3690.
25. Grantyn, A. (1989) How visual inputs to the ponto-bulbar reticular formation are used in the synthesis of premotor signals during orienting. Prog. Brain Res., 80, 159-170.
26. Grantyn, A. & Berthoz, A. (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Exp. Brain Res., 66, 339-354.
27. Graziano, M.S.A., Taylor, C.S.R. & Moore, T. (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron, 34, 841-851.
28. Grosbras, M.H. & Paus, T. (2002) Transcranial magnetic stimulation of the human frontal eye field: Effects on visual perception and attention. J. Cogn. Neurosci., 14, 1109-1120.
29. Guitton, D. & Mandl, G. (1978) Frontal oculomotor area in alert cat.1. Eye-movements and neck activity evoked by stimulation. Brain Res., 149, 295-312.
30. Hallett, M. (2007) Transcranial magnetic stimulation: a primer. Neuron, 55, 187-199.
31. Hanes, D.P. & Wurtz, R.H. (2001) Interaction of the frontal eye field and superior colliculus for saccade generation. J. Neurophysiol., 85, 804-815.
32. He, S.Q., Dum, R.P. & Strick, P.L. (1993) Topographic organization of corticospinal projections from the frontal-lobe - motor areas on the lateral surface of the hemisphere. J. Neurosci., 13, 952-980.
33. Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1987) Frontal eye field as defined by intracortical microstimulation in squirrel-monkeys, owl monkeys, and macaque monkeys. 2. Cortical connections. J. Comp. Neurol., 265, 332-361.
34. Isa, T. & Sasaki, S. (2002) Brainstem control of head movements during orienting; organization of the premotor circuits. Prog. Neurobiol., 66, 205-241.
35. Kamibayashi, L.K. & Richmond, F.J.R. (1998) Morphometry of human neck muscles. Spine, 23, 1314-1323.
36. Keshner, E.A., Campbell, D., Katz, R.T. & Peterson, B.W. (1989) Neck muscle activation patterns in humans during isometric head stabilization. Exp. Brain Res., 75, 335-344.
37. Knight, T.A. & Fuchs, A.F. (2007) Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation. J. Neurophysiol., 97, 618-634.
38. Logothetis, N.K., Augath, M., Murayama, Y., Rauch, A., Sultan, F., Goense, J., Oeltermann, A. & Merkle, H. (2010) The effects of electrical microstimulation on cortical signal propagation. Nat. Neurosci., 13, 1283-1291.
39. Mayoux-Benhamou, M.A., Revel, M. & Vallee, C. (1997) Selective electromyography of dorsal neck muscles in humans. Exp. Brain Res., 113, 353-360.
40. Monteon, J.A., Constantin, A.G., Wang, H., Martinez-Trujillo, J.C. & Crawford, J.D. (2010) Electrical stimulation of the frontal eye fields in the head-free macaque evokes kinematically normal 3D gaze shifts. J. Neurophysiol., 104, 3462-3475.
41. Moore, T. & Armstrong, K.M. (2003) Selective gating of visual signals by microstimulation of frontal cortex. Nature, 421, 370-373.
42. Muri, R.M., Hess, C.W. & Meienberg, O. (1991) Transcranial stimulation of the human frontal eye field by magnetic pulses. Exp. Brain Res., 86, 219-223.
43. O'Shea, J., Muggleton, N.G., Cowey, A. & Walsh, V. (2004) Timing of target discrimination in human frontal eye fields. J. Cogn. Neurosci., 16, 1060-1067.
44. Olk, B., Chang, E., Kingstone, A. & Ro, T. (2006) Modulation of antisaccades by transcranial magnetic stimulation of the human frontal eye field. Cereb. Cortex, 16, 76-82.
45. Opris, I., Barborica, A. & Ferrera, V.P. (2005) Microstimulation of the dorsolateral prefrontal cortex biases saccade target selection. J. Cogn. Neurosci., 17, 893-904.
46. Paus, T., Jech, R., Thompson, C.J., Comeau, R., Peters, T. & Evans, A.C. (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J. Neurosci., 17, 3178-3184.
47. Pélisson, D., Goffart, L., Guillaume, A., Catz, N. & Raboyeau, G. (2001) Early head movements elicited by visual stimuli or collicular electrical stimulation in the cat. Vision Res., 41, 3283-3294.
48. Petit, L. & Beauchamp, M.S. (2003) Neural basis of visually guided head movements studied with fMRI. J. Neurophysiol., 89, 2516-2527.
49. Rasmussen, T. & Penfield, W. (1947) Movement of head and eyes from stimulation of human frontal cortex. Res. Publ. Assoc. Res. Nerv. Ment. Dis., 27, 346-361.
50. Rezvani, S. & Corneil, B.D. (2008) Recruitment of a head-turning synergy by low-frequency activity in the primate superior colliculus. J. Neurophysiol., 100, 397-411.
51. Richmond, F.J.R., Singh, K. & Corneil, B.D. (2001) Neck muscles in the rhesus monkey. I. Muscle morphometry and histochemistry. J. Neurophysiol., 86, 1717-1728.
52. Ruff, C.C., Blankenburg, F., Bjoertomt, O., Bestmann, S., Freeman, E., Haynes, J.D., Rees, G., Josephs, O., Deichmann, R. & Driver, J. (2006) Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr. Biol., 16, 1479-1488.
53. Schall, J.D. (2002) The neural selection and control of saccades by the frontal eye field. Philos. Trans. R. Soc. Lond., B, Biol. Sci., 357, 1073-1082.
54. Schiller, P.H., True, S.D. & Conway, J.L. (1979) Effects of frontal eye field and superior colliculus ablations on eye-movements. Science, 206, 590-592.
55. Schiller, P.H., True, S.D. & Conway, J.L. (1980) Deficits in eye-movements following frontal eye-field and superior colliculus ablations. J. Neurophysiol., 44, 1175-1189.
56. Schnyder, H., Reisine, H., Hepp, K. & Henn, V. (1985) Frontal eye field projection to the paramedian pontine reticular-formation traced with wheat-germ agglutinin in the monkey. Brain Res., 329, 151-160.
57. Scudder, C.A., Kaneko, C.R.S. & Fuchs, A.F. (2002) The brainstem burst generator for saccadic eye movements - a modern synthesis. Exp. Brain Res., 142, 439-462.
58. Segraves, M.A. (1992) Activity of monkey frontal eye field neurons projecting to the oculomotor regions of the pons. J. Neurophysiol., 68, 1967-1985.
59. Segraves, M.A. & Goldberg, M.E. (1987) Functional-properties of corticotectal neurons in the monkeys frontal eye field. J. Neurophysiol., 58, 1387-1419.
60. Silvanto, J., Lavie, N. & Walsh, V. (2006) Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. J. Neurophysiol., 96, 941-945.
61. Smith, D.T., Jackson, S.R. & Rorden, C. (2005) Transcranial magnetic stimulation of the left human frontal eye fields eliminates the cost of invalid endogenous cues. Neuropsychologia, 43, 1288-1296.
62. Sommer, M.A. & Wurtz, R.H. (2000) Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J. Neurophysiol., 83, 1979-2001.
63. Stanton, G.B., Bruce, C.J. & Goldberg, M.E. (1993) Topography of projections to the frontal-lobe from the macaque frontal eye fields. J. Comp. Neurol., 330, 286-301.
64. Tark, K.J. & Curtis, C.E. (2009) Persistent neural activity in the human frontal cortex when maintaining space that is off the map. Nat. Neurosci., 12, 1463-1468.
65. Taylor, P.C.J., Nobre, A.C. & Rushworth, M.F.S. (2007) FEF TMS affects visual cortical activity. Cereb. Cortex, 17, 391-399.
66. Tehovnik, E.J., Sommer, M.A., Chou, I.H., Slocum, W.M. & Schiller, P.H. (2000) Eye fields in the frontal lobes of primates. Brain Res. Rev., 32, 413-448.
67. Thompson, M.L., Thickbroom, G.W. & Mastaglia, F.L. (1997) Corticomotor representation of the sternocleidomastoid muscle. Brain, 120, 245-255.
68. Tu, T.A. & Keating, E.G. (2000) Electrical stimulation of the frontal eye field in a monkey produces combined eye and head movements. J. Neurophysiol., 84, 1103-1106.
69. Vasavada, A.N., Li, S.P. & Delp, S.L. (1998) Influence of muscle morphometry and moment arms on the moment-generating capacity of human neck muscles. Spine, 23, 412-422.
70. Wessel, K. & Kömpf, D. (1991) Transcranial magnetic brain-stimulation - lack of oculomotor response. Exp. Brain Res., 86, 216-218.
71. Wessel, K., Kömpf, D., Klostermann, W. & Moser, A. (1991) Lack of oculomotor response after transcranial magnetic stimulation. Neuro-Ophthalmology, 11, 199-208.
72. Wipfli, M., Felblinger, J., Mosimann, U.P., Hess, C.W., Schlaepfer, T.E. & Muri, R.M. (2001) Double-pulse transcranial magnetic stimulation over the frontal eye field facilitates triggering of memory-guided saccades. Eur. J. Neurosci., 14, 571-575.
73. Zangemeister, W.H. & Stark, L. (1982) Gaze latency - variable interactions of head and eye latency. Exp. Neurol., 75, 389-406.
74. Zangemeister, W.H., Stark, L., Meienberg, O. & Waite, T. (1982) Neural control of head rotation - electro-myographic evidence. J. Neurol. Sci., 55, 1-14.
75. Zangemeister, W.H., Canavan, A.G.M. & Hoemberg, V. (1995) Frontal and parietal transcranial magnetic stimulation (TMS) disturbs programming of saccadic eye-movements. J. Neurol. Sci., 133, 42-52.