Abstract
Eye movements exhibit reduced latencies when the point of fixation is extinguished prior to, or coincident with, the appearance of a peripheral target. Two independent components are responsible for this facilitation. If the offset occurs before target onset, it presents a warning which stimulates response preparation and execution. If offset occurs prior to or coincident with target onset, it triggers the release of fixation-maintenance neurons in the superior colliculus that can delay saccadic responses. While the warning effect facilitates responses regardless of effector, the fixation release effect is thought to be specific to the oculomotor system. Head movements, like saccades, contribute significantly to gaze shifts and may be generated directly by the SC. While head movements have been shown to benefit from the warning effect, it is unknown if, and to what degree, they are affected by the release of fixation-maintenance neurons responsible for inhibiting saccades. To address this issue, we measured head and eye response latencies in a virtual reality-based gap paradigm, turning off the fixation point either 200 ms before (temporal gap condition), coincident with (step condition), or 1000 ms after (temporal overlap/baseline condition) target onset. Our results indicate that head movements, like saccades, are facilitated by both the warning and release components of the gap paradigm. Further, rotational kinematics during gap trials differed significantly from those observed in step and overlap trials (higher, earlier peak velocities). These results are discussed with respect to the theorized structure and organisation of the superior colliculus in humans.
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Andersson R, Larsson L, Holmqvist K, Stridh M, Nyström M (2017) One algorithm to rule them all? An evaluation and discussion of ten eye movement event-detection algorithms. Behav Res Methods 49(2):616–637
Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004) Prepared movements are elicited early by startle. J Mot Behav 36(3):253–264
Carpenter R (2001) Express saccades: is bimodality a result of the order of stimulus presentation? Vis Res 41(9):1145–1151
Corneil BD, Munoz DP (1999) Human eye-head gaze shifts in a distractor task. II. Reduced threshold for initiation of early head movements. J Neurophysiol 82(3):1406–1421
Corneil BD, Olivier E, Munoz DP (2002a) Neck muscle responses to stimulation of monkey superior colliculus. I. Topography and manipulation of stimulation parameters. J Neurophysiol 88(4):1980–1999
Corneil BD, Olivier E, Munoz DP (2002b) Neck muscle responses to stimulation of monkey superior colliculus. II. Gaze shift initiation and volitional head movements. J Neurophysiol 88(4):2000–2018
Corneil BD, Olivier E, Munoz DP (2004) Visual responses on neck muscles reveal selective gating that prevents express saccades. Neuron 42(5):831–841
Corneil BD, Munoz DP, Olivier E (2007) Priming of head premotor circuits during oculomotor preparation. J Neurophysiol 97(1):701–714
Corneil BD, Munoz DP, Chapman BB, Admans T, Cushing SL (2008) Neuromuscular consequences of reflexive covert orienting. Nat Neurosci 11(1):13–15
Crapse TB, Sommer MA (2009) Frontal eye field neurons with spatial representations predicted by their subcortical input. J Neurosci 29(16):5308–5318
Dorris MC, Munoz DP (1995) A neural correlate for the gap effect on saccadic reaction times in monkey. J Neurophysiol 73(6):2558–2562
Faulkner RF, Hyde JE (1958) Coordinated eye and body movements evoked by brainstem stimulation in decerebrated cats. J Neurophysiol 21(2):171–182
Fischer B, Weber H (1993) Express saccades and visual attention. Behav Brain Sci 16(3):553–567
Freedman EG, Stanford TR, Sparks DL (1996) Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J Neurophysiol 76(2):927–952
Galiana H, Guitton D (1992) Central Organization and Modeling of Eye-Head Coordination during Orienting Gaze Shifts a. Ann N Y Acad Sci 656(1):452–471
Goldring JE, Dorris MC, Corneil BD, Ballantyne PA, Munoz DR (1996) Combined eye-head gaze shifts to visual and auditory targets in humans. Exp Brain Res 111(1):68–78
Goonetilleke SC, Katz L, Wood DK, Gu C, Huk AC, Corneil BD (2015) Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates. J Neurophysiol 114(2):902–913
Kingstone A, Klein RM (1993a) Visual offsets facilitate saccadic latency: does predisengagement of visuospatial attention mediate this gap effect? J Exp Psychol Hum Percept Perform 19(6):1251
Kingstone A, Klein RM (1993b) What are human express saccades? Percept Psychophys 54(2):260–273
Land MF (2004) The coordination of rotations of the eyes, head and trunk in saccadic turns produced in natural situations. Exp Brain Res 159(2):151–160
Lubetzky AV, Wang Z, Krasovsky T (2019) Head mounted displays for capturing head kinematics in postural tasks. J Biomech 86:175–182
Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218
Munoz DP, Fecteau JH (2002) Vying for dominance: dynamic interactions control visual fixation and saccadic initiation in the superior colliculus. Prog Brain Res 140:3–19. https://doi.org/10.1016/s0079-6123(02)40039-8
Nichols S (1999) Physical ergonomics of virtual environment use. Appl Ergon 30(1):79–90
Reuter-Lorenz PA, Hughes HC, Fendrich R (1991) The reduction of saccadic latency by prior offset of the fixation point: an analysis of the gap effect. Percept Psychophys 49(2):167–175
Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12(11):1795–1808
Ross SM, Ross LE (1980) Saccade latency and warning signals: stimulus onset, offset, and change as warning events. Percept Psychophys 27(3):251–257
Ross SM, Ross LE (1981) Saccade latency and warning signals: effects of auditory and visual stimulus onset and offset. Percept Psychophys 29(5):429–437
Roucoux A, Crommelinck M (1976) Eye movements evoked by superior colliculus stimulation in the alert cat. Brain Res 106:349
Saslow M (1967) Effects of components of displacement-step stimuli upon latency for saccadic eye movement. Josa 57(8):1024–1029
Stahl JS (1999) Amplitude of human head movements associated with horizontal saccades. Exp Brain Res 126(1):41–54
Suzuki T, Hirai N (1998) Reaction times of head movements occurring in association with express saccades during human gaze shifts. Neurosci Lett 254(1):61–64
Tomlinson R, Bahra P (1986) Combined eye-head gaze shifts in the primate. I Metrics. J Neurophysiol 56(6):1542–1557
Uemura T, Arai Y, Shimazaki C (1980) Eye-head coordination during lateral gaze in normal subjects. Acta Otolaryngol 90(1–6):191–198
Viviani P, Swensson RG (1982) Saccadic eye movements to peripherally discriminated visual targets. J Exp Psychol Hum Percept Perform 8(1):113
Warabi T (1977) The reaction time of eye-head coordination in man. Neurosci Lett 6(1):47–51
Xu X, Chen KB, Lin J-H, Radwin RG (2015) The accuracy of the Oculus Rift virtual reality head-mounted display during cervical spine mobility measurement. J Biomech 48(4):721–724
Zangemeister W, Stark L (1982) Types of gaze movement: variable interactions of eye and head movements. Exp Neurol 77(3):563–577
Acknowledgement
This study was conducted with support from the National Science and Engineering Research Council of Canada (NSERC; Grant no. PDF-51673-2018). Data and analysis code can be found at https://osf.io/9nfmb/?view_only=95e83f82a7444f9983f0f54d2bd9b137
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Communicated by Melvyn A. Goodale.
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Flindall, J., Sara, A. & Kingstone, A. Head and eye movements are each facilitated by the offset of a central fixation point in a virtual gap paradigm. Exp Brain Res 239, 117–126 (2021). https://doi.org/10.1007/s00221-020-05905-9
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DOI: https://doi.org/10.1007/s00221-020-05905-9