TMS perturbs saccade trajectories and unmasks an internal feedback controller for saccades

Journal of Neuroscience

Volumn 31, Issue 32, 2011, Pages 11537-11546

  Xu Wilson, Minnan ^a   Tian, Jing ^a   Shadmehr, Reza ^a   Zee, David S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; EXTRAOCULAR MUSCLE; EYE MOVEMENT CONTROL; EYE POSITION; EYELID; FEEDBACK SYSTEM; FEMALE; HABITUATION; HUMAN; HUMAN EXPERIMENT; MALE; MOTONEURON; MOTOR COORDINATION; NORMAL HUMAN; OCULOMOTOR SYSTEM; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; STARTLE REFLEX; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; FEEDBACK, PHYSIOLOGICAL; FEMALE; HUMANS; MALE; PHOTIC STIMULATION; SACCADES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 80051576118     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1584-11.2011     Document Type: Article

References (46)

1. Arai K, Das S, Keller EL, Aiyoshi E (1999) Adistributed model of the saccade system: simulations of temporally perturbed saccades using position and velocity feedback. Neural Netw 12:1359-1375.
2. Becker W (1993) Banging the bang-bang circuit: experimental test of Robinson's local feedback theory of saccade generation. In: Contemporary ocular motor and vestibular research: a tribute to David A. Robinson (Fuchs AF, Brandt T, Buttner U, Zee DS, eds), pp 496-503. New York: Thieme.
3. Becker W, Fuchs AF (1988) Lid-eye coordination during vertical gaze changes in man and monkey. J Neurophysiol 60:1227-1252.
4. Bhushan N, Shadmehr R (1999) Evidence for learning of a forward dynamic model in human motor control. In: Advances in neural information processing systems 11 (Kearns MS, Kearns MS, eds). Cambridge, MA: MIT.
5. Bischoff C, Liscic R, Meyer BU, Machetanz J, Conrad B (1993) Magnetically elicited blink reflex: an alternative to conventional electrical stimulation. Electromyogr Clin Neurophysiol 33:265-269.
6. Braff DL, Geyer MA, Swerdlow NR (2011) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156:234-258.
7. Büttner-Ennever JA, Horn AK (2004) Reticular formation: eye movements, gaze, and blinks. In: The human nervous system (Paxinos G, Mai JK, eds), pp 479-510. Amsterdam: Elsevier.
8. Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2003) Startle response is dishabituated during a reaction time task. Exp Brain Res 152:510-518.
9. Carlsen AN, Maslovat D, Lam MY, Chua R, Franks IM (2011) Considerations for the use of a startling acoustic stimulus in studies of motor preparation in humans. Neurosci Biobehav Rev 35:366-376.
10. Castellote JM, Kumru H, Queralt A, Valls-Solé J (2007) A startle speeds up the execution of externally guided saccades. Exp Brain Res 177:129-136.
11. Dean P, Redgrave P, WestbyGW (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137-147.
12. Enderle JD (2002) Neural control of saccades. In: The brain's eye: neurobiological and clinical aspects of oculomotor research (Progress in brain research) (Hyönä J, Munoz DP, Heide W, eds), pp 21-49. Oxford: Elsevier.
13. Epelboim J, Steinman RM, Kowler E, Pizlo Z, Erkelens CJ, Collewijn H (1997) Gaze-shift dynamics in two kinds of sequential looking tasks. Vision Res 37:2597-2607.
14. Evinger C, Kaneko CR, Fuchs AF (1982) Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J Neurophysiol 47:827-844.
15. Gandhi NJ, Keller EL (1999) Activity of the brain stem omnipause neurons during saccades perturbed by stimulation of the primate superior colliculus. J Neurophysiol 82:3254-3267.
16. Geyer MA, Swerdlow NR (1998) Measurement of startle response, prepulse inhibition, and habituation. In: Current protocols in neuroscience (Crawley JN, Skolnick P, eds). New York: Wiley.
17. Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, Thier P (2008) Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur J Neurosci 27:132-144.
18. Goossens HH, Van Opstal AJ (2000) Blink-perturbed saccades in monkey. II. Superior colliculus activity. J Neurophysiol 83:3430-3452.
19. Goossens HH, van Opstal AJ (2010) Differential effects of reflex blinks on saccade perturbations in humans. J Neurophysiol 103:1685-1695.
20. Guthrie BL, Porter JD, Sparks DL (1983) Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193-1195.
21. Hashimoto M, Ohtsuka K (1995) Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain 118:1185-1193.
22. Izawa J, Shadmehr R (2008) On-line processing of uncertain information in visuomotor control. J Neurosci 28:11360-11368.
23. Keller EL, Edelman JA (1994) Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. J Neurophysiol 72:2754-2770.
24. Keller EL, Slakey DP, Crandall WF (1983) Microstimulation of the primate cerebellar vermis during saccadic eye movements. Brain Res 288:131-143.
25. Keller EL, Gandhi NJ, Shieh JM (1996) Endpoint accuracy in saccades interrupted by stimulation in the omnipause region in monkey. Vis Neurosci 13:1059-1067.
26. Keller EL, Gandhi NJ, Vijay Sekaran S (2000) Activity in deep intermediate layer collicular neurons during interrupted saccades. Exp Brain Res 130:227-237.
27. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59:107-128.
28. Langer TP, Kaneko CR (1990) Brainstem afferents to the oculomotor omnipause neurons in monkey. J Comp Neurol 295:413-427.
29. Lin C, Wan X, Zhao W, Ma C, Ma C, Gao Y, Zhou Y, Yeomans JS, Li L (2002) Enhancement of electrically evoked startle-like responses by tetanic stimulation of the superior colliculus. Neuroreport 13:1769-1773.
30. Miura K, Optican LM (2006) Membrane channel properties of premotor excitatory burst neurons may underlie saccade slowing after lesions of omnipause neurons. J Comput Neurosci 20:25-41.
31. Munoz DP, Waitzman DM, Wurtz RH (1996) Activity of neurons in monkey superior colliculus during interrupted saccades. J Neurophysiol 75:2562-2580.
32. Optican LM, Robinson DA (1980) Cerebellar-dependent adaptive control of primate saccadic system. J Neurophysiol 44:1058-1076.
33. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83:117-161.
34. Quaia C, Lefevre P, Optican LM (1999) Model of the control of saccades by superior colliculus and cerebellum. J Neurophysiol 82:999-1018.
35. Ramat S, Leigh RJ, Zee DS, Optican LM (2005) Ocular oscillations generated by coupling of brainstem excitatory and inhibitory saccadic burst neurons. Exp Brain Res 160:89-106.
36. Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137-145.
37. Robinson DA (1975) Oculomotor control signals. In: Basic mechanisms of ocular motility and their clinical implications (BachyRita P, Lennerstrand G, eds), pp 337-374. Oxford, UK: Pergamon.
38. Shaikh AG, Wong AL, Optican LM, Miura K, Solomon D, Zee DS (2010) Sustained eye closure slows saccades. Vision Res 50:1665-1675.
39. Siebner HR, Auer C, Roeck R, Conrad B (1999) Trigeminal sensory input elicited by electric or magnetic stimulation interferes with the central motor drive to the intrinsic hand muscles. Clin Neurophysiol 110:1090-1099.
40. Soetedjo R, Kaneko CR, Fuchs AF (2002) Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J Neurophysiol 87:679-695.
41. Straube A, Robinson FR, Fuchs AF (1997) Decrease in saccadic performance after many visually guided saccadic eye movements in monkeys. Invest Ophthalmol Vis Sci 38:2810-2816.
42. Valls-Solé J, Rothwell JC, Goulart F, Cossu G, Muñoz E (1999) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516:931-938.
43. Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R (2009a) Cerebellar contributions to adaptive control of saccades in humans. J Neurosci 29:12930-12939.
44. Xu-Wilson M, Zee DS, Shadmehr R (2009b) The intrinsic value of visual information affects saccade velocities. Exp Brain Res 196:475-481.
45. Yeomans JS, Li L, Scott BW, Frankland PW (2002) Tactile, acoustic and vestibular systems sum to elicit the startle reflex. Neurosci Biobehav Rev 26:1-11.
46. Zee DS, Optican LM, Cook JD, Robinson DA, Engel WK (1976) Slow saccades in spinocerebellar degeneration. Arch Neurol 33:243-251.