Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze-reach movements

European Journal of Neuroscience

Volumn 34, Issue 12, 2011, Pages 1966-1982

  Reyes Puerta, Vicente ^a,b   Philipp, Roland ^a,c   Lindner, Werner ^a   Hoffmann, Klaus Peter ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Eye hand coordination; Fixation; Monkey; Reaching; Saccade

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARM MOVEMENT; ARTICLE; CONTROLLED STUDY; EYE FIXATION; EYE HAND COORDINATION; FRONTAL EYE FIELD; GAZE; LATENT PERIOD; MALE; NERVE CELL; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; REACTION TIME; RHESUS MONKEY; SACCADIC EYE MOVEMENT; SPIKE; SUPERIOR COLLICULUS; TASK PERFORMANCE;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; HUMANS; MACACA MULATTA; MALE; MOVEMENT; NEURONS; REACTION TIME; SACCADES; SUPERIOR COLLICULI;

EID: 83555179060     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07911.x     Document Type: Article

References (61)

1. Aizawa, H., Kobayashi, Y., Yamamoto, M. & Isa, T. (1999) Injection of nicotine into the superior colliculus facilitates occurrence of express saccades in monkeys. J. Neurophysiol., 82, 1642-1646.
2. Andersen, R.A. & Buneo, C.A. (2002) Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci., 25, 189-220.
3. Ariff, G., Donchin, O., Nanayakkara, T. & Shadmehr, R. (2002) A real-time state predictor in motor control: study of saccadic eye movements during unseen reaching movements. J. Neurosci., 22, 7721-7729.
4. Baker, J.T., Donoghue, J.P. & Sanes, J.N. (1999) Gaze direction modulates finger movement activation patterns in human cerebral cortex. J. Neurosci., 19, 10044-10052.
5. Basso, M.A. & Wurtz, R.H. (1998) Modulation of neuronal activity in superior colliculus by changes in target probability. J. Neurosci., 18, 7519-7534.
6. Batista, A.P., Buneo, C.A., Snyder, L.H. & Andersen, R.A. (1999) Reach plans in eye-centered coordinates. Science, 285, 257-260.
7. Bell, A.H., Meredith, M.A., Van Opstal, A.J. & Munoz, D.P. (2006) Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus. Exp. Brain Res., 174, 53-59.
8. Bowman, M.C., Johannson, R.S. & Flanagan, J.R. (2009) Eye-hand coordination in a sequential target contact task. Exp. Brain Res., 195, 273-283.
9. Choi, W.Y. & Guitton, D. (2006) Responses of collicular fixation neurons to gaze shift perturbations in head-unrestrained monkey reveal gaze feedback control. Neuron, 50, 1-15.
10. Crawford, J.D., Medendorp, W.P. & Marotta, J.J. (2004) Spatial transformations for eye-hand coordination. J. Neurophysiol., 92, 10-19.
11. Dorris, M.C. & Munoz, D.P. (1995) A neural correlate for the gap effect on saccadic reaction times. J. Neurophysiol., 73, 2558-2562.
12. Dorris, M.C. & Munoz, D.P. (1998) Saccadic probability influences motor preparation signals and time to saccadic initiation. J. Neurosci., 18, 7015-7026.
13. Dorris, M.C., Paré, M. & Munoz, D.P. (1997) Neural activity in superior colliculus related to the initiation of saccadic eye movements. J. Neurosci., 17, 8566-8579.
14. Edelman, J.A. & Keller, E.L. (1996) Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. J. Neurophysiol., 76, 908-926.
15. Epelboim, J., Steinman, R.M., Kowler, E., Pizlo, Z., Erkelens, C.J. & Collewijn, H. (1997) Gaze-shift dynamics in two kinds of sequential looking tasks. Vision Res., 37, 2597-2607.
16. Everling, S., Dorris, M.C., Klein, R.M. & Munoz, D.P. (1999) Role of Primate Superior Colliculus in Preparation and Execution of Anti-Saccades and Pro-Saccades. J. Neurosci., 19, 2740-2754.
17. Frens, M.A. & Van Opstal, A.J. (1998) Visual-auditory interactions modulate saccade-related activity in monkey superior colliculus. Brain Res. Bull., 46, 211-224.
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. Fries, W. (1985) Inputs from motor and premotor cortex to the superior colliculus of the macaque monkey. Behav. Brain Res., 18, 95-105.
20. Goossens, H.H.L.M. & Van Opstal, A.J. (2000) Blink-perturbed saccades in monkey. II. Superior colliculus activity. J. Neurophysiol., 83, 3430-3452.
21. Gowen, E. & Miall, R.C. (2006) Eye-hand interactions in tracing and drawing tasks. Hum. Mov. Sci., 25, 568-585.
22. Hanes, D.P. & Wurtz, R.H. (2001) Interaction of the frontal eye field and superior colliculus for saccade generation. J. Neurophysiol., 85, 804-815.
23. Helsen, W.F., Starkes, J.L., Elliott, D. & Ricker, K.L. (1998) Temporal and spatial coupling of point of gaze and hand movements in aiming. J. Mot. Behav., 30, 249-259.
24. Horstmann, A. & Hoffmann, K.P. (2005) Target selection in eye-hand coordination: do we reach to where we look or do we look to where we reach?. Exp. Brain Res., 167, 187-195.
25. Johansson, R.S., Westling, G., Bäckström, A. & Flanagan, J.R. (2001) Eye-hand coordination in object manipulation. J. Neurosci., 21, 6917-6932.
26. Judge, S.J., Richmond, B.J. & Chu, F.C. (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res., 20, 535-538.
27. Karnath, H.O. & Perenin, M.T. (2005) Cortical control of visually guided reaching: evidence from patients with optic ataxia. Cereb. Cortex, 15, 1561-1569.
28. Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. (2000) Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J. Neurophysiol., 84, 876-891.
29. Liesker, H., Brenner, E. & Smeets, J.B.J. (2009) Combining eye and hand in search is suboptimal. Exp. Brain Res., 197, 395-401.
30. Lünenburger, L. & Hoffmann, K.P. (2003) Arm movement and gap as factors influencing the reaction time of the second saccade in a double-step task. Eur. J. Neurosci., 17, 2481-2491.
31. Lünenburger, L., Kutz, D.F. & Hoffmann, K.P. (2000) Influence of arm movements on saccades in humans. Eur. J. Neurosci., 12, 4107-4116.
32. McPeek, R.M. & Keller, E.L. (2002) Superior colliculus activity related to concurrent processing of saccade goals in a visual search task. J. Neurophysiol., 87, 1805-1815.
33. Munoz, D.P. & Istvan, P.J. (1998) Lateral inhibitory interactions in the intermediate layers of the superior colliculus. J. Neurophysiol., 79, 1193-1209.
34. Munoz, D.P. & Wurtz, R.H. (1993a) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J. Neurophysiol., 70, 559-575.
35. Munoz, D.P. & Wurtz, R.H. (1993b) Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J. Neurophysiol., 70, 576-589.
36. Munoz, D.P. & Wurtz, R.H. (1995a) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol., 73, 2313-2333.
37. Munoz, D.P. & Wurtz, R.H. (1995b) Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol., 73, 2334-2348.
38. Mushiake, H., Fujii, N. & Tanji, J. (1996) Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields. J. Neurophysiol., 75, 2187-2191.
39. Mushiake, H., Tanatsugu, Y. & Tanji, J. (1997) Neuronal activity in the ventral part of premotor cortex during target-reach movement is modulated by direction of gaze. J. Neurophysiol., 78, 567-571.
40. Nagy, A., Kruse, W., Rottmann, S., Dannenberg, S. & Hoffmann, K.P. (2006) Somatosensory-motor neuronal activity in the superior colliculus of the primate. Neuron, 52, 525-534.
41. Neggers, S.F.W. & Bekkering, H. (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J. Neurophysiol., 83, 639-651.
42. Neggers, S.F.W. & Bekkering, H. (2001) Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. J. Neurophysiol., 86, 961-970.
43. Paré, M. & Hanes, D.P. (2003) Controlled movement processing: superior colliculus activity associated with countermanded saccades. J. Neurosci., 23, 6480-6489.
44. Pesaran, B., Nelson, M.J. & Andersen, R.A. (2010) A relative position Code for saccades in the dorsal premotor cortex. J. Neurosci., 30, 6527-6537.
45. Prado, J., Clavagnier, S., Otzenberger, H., Scheiber, C., Kennedy, H. & Perenin, M. (2005) Two Cortical Systems for Reaching in Central and Peripheral Vision. Neuron, 48, 849-858.
46. Reyes-Puerta, V., Philipp, R., Lindner, W., Lünenburger, L. & Hoffmann, K.P. (2009) Influence of task predictability on the activity of neurons in the rostral superior colliculus during double-step saccades. J. Neurophysiol., 101, 3199-3211.
47. Reyes-Puerta, V., Philipp, R., Lindner, W. & Hoffmann, K.P. (2010) Role of the rostral superior colliculus in gaze anchoring during reach movements. J. Neurophysiol., 103, 3153-3166.
48. Rushworth, M.F.S., Nixon, P.D. & Passingham, R.E. (1997) Parietal cortex and movement I. Movement selection and reaching. Exp. Brain Res., 117, 292-310.
49. 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.
50. Snyder, L.H., Calton, J.L., Dickinson, A.R. & Lawrence, B.M. (2002) Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. J. Neurophysiol., 87, 2279-2286.
51. Sparks, D.L. (1978) Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res., 156, 1-16.
52. Sparks, D.L. & Hartwich-Young, R. (1989) The deep layers of the superior colliculus. In Wurtz, R.H. & Goldberg, M.E. (Eds), The Neurobiology of Saccadic Eye Movements. Elsevier, Amsterdam, pp. 213-255.
53. Sparks, D., Rohrer, W.H. & Zhang, Y. (2000) The role of the superior colliculus in saccade initiation: a study of express saccades and the gap effect. Vision Res., 40, 2763-2777.
54. Stuphorn, V., Hoffmann, K.P. & Miller, L.E. (1999) Correlation of primate superior colliculus and reticular formation discharge with proximal limb muscle activity. J. Neurophysiol., 81, 1978-1982.
55. Stuphorn, V., Bauswein, E. & Hoffmann, K.P. (2000) Neurons in the primate superior colliculus coding for arm movements in gaze-related coordinates. J. Neurophysiol., 83, 1283-1299.
56. Thura, D., Hadj-Bouziane, F., Meunier, M. & Boussaoud, D. (2008) Hand position modulates saccadic activity in the frontal eye field. Behav. Brain Res., 186, 148-153.
57. Vidoni, E.D., McCarley, J.S., Edwards, J.D. & Boyd, L.A. (2009) Manual and oculomotor performance develop contemporaneously but independently during continuous tracking. Exp. Brain Res., 195, 611-620.
58. Werner, W. (1993) Neurons in the primate superior colliculus are active before and during arm movements to visual targets. Eur. J. Neurosci., 5, 335-340.
59. Werner, W., Dannenberg, S. & Hoffmann, K.P. (1997a) Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching. Exp. Brain Res., 115, 191-205.
60. Werner, W., Hoffmann, K.P. & Dannenberg, S. (1997b) Anatomical distribution of arm-movement-related neurons in the primate superior colliculus and underlying reticular formation in comparison with visual and saccadic cells. Exp. Brain Res., 115, 206-216.
61. Zar, J.H. (1999) Biostatistical Analysis, 4th Edn. Prentice Hall, New Jersey.