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Neural network simulations of the primate oculomotor system. V. Eye–head gaze shifts

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Abstract

We examined the performance of a dynamic neural network that replicates much of the psychophysics and neurophysiology of eye–head gaze shifts without relying on gaze feedback control. For example, our model generates gaze shifts with ocular components that do not exceed 35° in amplitude, whatever the size of the gaze shifts (up to 75° in our simulations), without relying on a saturating nonlinearity to accomplish this. It reproduces the natural patterns of eye–head coordination in that head contributions increase and ocular contributions decrease together with the size of gaze shifts and this without compromising the accuracy of gaze realignment. It also accounts for the dependence of the relative contributions of the eyes and the head on the initial positions of the eyes, as well as for the position sensitivity of saccades evoked by electrical stimulation of the superior colliculus. Finally, it shows why units of the saccadic system could appear to carry gaze-related signals even if they do not operate within a gaze control loop and do not receive head-related information.

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References

  • Azuma M, Kodaka Y, Shindo J-I, Suzuki H (1996) Effects of eye position on saccades evoked by stimulation of the monkey superior colliculus. Neuroreport 7: 2287–2292

    Article  CAS  PubMed  Google Scholar 

  • Becker W, Jürgens R (1992) Gaze saccades to visual targets: does head movement change the metrics?. In: Berthoz A, Graf W, Vidal P-P (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 427–433

    Google Scholar 

  • Bizzi E (1978) Strategies of eye-head coordination. In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Elsevier, Amsterdam, pp 795–803

    Google Scholar 

  • Bizzi E (1981) Eye-head coordination. In: Brooks V (eds) Handbook of physiology: the nervous system. American Physiological Society, Bethesda, pp 1321–1336

    Google Scholar 

  • Bizzi E, Dev P, Morasso P, Polit A (1978) Effect of load disturbances during centrally initiated movements. J Neurophysiol 41: 542–556

    CAS  PubMed  Google Scholar 

  • Bozis A, Moschovakis AK (1998) Neural network simulations of the primate oculomotor system. III. A one-dimensional one-directional model of the superior colliculus. Biol Cybern 79: 215–230

    Article  CAS  PubMed  Google Scholar 

  • Collewijn H, Steinman RM, Erkelens CJ, Pizio Z, van der Steen J (1992) Effect of freeing the head on eye movement characteristics during three-dimensional shifts of gaze and tracking. In: Berthoz A, Graf W, Vidal P-P (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 412–418

    Google Scholar 

  • Corneil BD, Olivier E, Munoz DP (2002) Neck muscle responses to stimulation of monkey superior colliculus. I. Topography and manipulation of stimulation parameters. J Neurophysiol 88: 1980–1999

    PubMed  Google Scholar 

  • Cullen KE, Guitton D (1997) Analysis of primate IBN spike trains using system identification techniques. III. Relationship to motor error during head-fixed saccades and head-free gaze shifts. J Neurophysiol 78: 3307–3322

    CAS  PubMed  Google Scholar 

  • Cullen KE, Galiana HL, Sylvestre PA (2000) Comparing extraocular motoneuron discharges during head-restrained saccades and head-unrestrained gaze shifts. J Neurophysiol 83: 630–637

    CAS  PubMed  Google Scholar 

  • Cullen KE, Huterer M, Braidwood DA, Sylvestre PA (2004) Time course of vestibuloocular reflex suppression during gaze shifts. J Neurophysiol 92: 3408–3422

    Article  PubMed  Google Scholar 

  • Freedman EG (2001) Interactions between eye and head control signals can account for movement kinematics. Biol Cybern 84: 453–462

    Article  CAS  PubMed  Google Scholar 

  • Freedman EG, Quessy S (2004) Electrical stimulation of rhesus monkey reticularis gigantocellularis. II. Effects on metrics and kinematics of ongoing gaze shifts to visual targets. Exp Brain Res 156: 357–376

    Article  PubMed  Google Scholar 

  • Freedman EG, Sparks DL (1997a) Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. J Neurophysiol 78: 1669–1690

    CAS  PubMed  Google Scholar 

  • Freedman EG, Sparks DL (1997b) Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77: 2328–2348

    CAS  PubMed  Google Scholar 

  • Grantyn A, Berthoz A (1987) Reticulospinal 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

    Article  CAS  PubMed  Google Scholar 

  • Grantyn A, Hardy O, Olivier E, Gourdon A (1992) Relationship between task-related discharge patterns and axonal morphology of brainstem projection neurons involved in orienting eye and head movements. In: Shimazu H, Shinoda Y (eds) Vestibular and brain stem control of eye, head and body movements. Japan Scientific Societies Press, Tokyo, pp 255–273

    Google Scholar 

  • Grantyn AA, Dalezios Y, Kitama T, Moschovakis AK (1996) Neuronal mechanisms of two-dimensional orienting movements in the cat. I. A quantitative study of saccades and slow drifts produced in response to the electrical stimulation of the superior colliculus. Brain Res Bull 41: 65–82

    Article  CAS  PubMed  Google Scholar 

  • Grantyn A, Brandi A-M, Dubayle D, Graf W, Ugolini G, Hadjidimitrakis K, Moschovakis A (2002a) Density gradients of trans-synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey. J Comp Neurol 451: 346–361

    Article  PubMed  Google Scholar 

  • Grantyn A, Kuze B, Brandi A-M, Thomas M-A. (2002b) Contribution of pontine omnipause neurons (OPN) to eye-head coordination in the cat. In: Proceedings of the XXII meeting of the Barany Society, p 9.3

  • Guitton D, Crommelinck M, Roucoux A (1980) Stimulation of the superior colliculus in the alert cat. I. Eye movements and neck EMG activity evoked when the head is restrained. Exp Brain Res 39: 63–73

    Article  CAS  PubMed  Google Scholar 

  • Guitton D, Douglas RM, Volle M (1984) Eye-head coordination in cats. J Neurophysiol 52: 1030–1050

    CAS  PubMed  Google Scholar 

  • Guitton D, Munoz DP, Galiana HL (1990) Gaze control in the cat: Studies and modeling of the coupling between orienting eye and head movements in different behavioral tasks. J Neurophysiol 64: 509–531

    CAS  PubMed  Google Scholar 

  • Guitton D, Volle M (1987) Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58: 427–459

    CAS  PubMed  Google Scholar 

  • Hadjidimitrakis K, Moschovakis AK, Dalezios Y, Grantyn A (2007) Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat. Exp Brain Res 179: 1–16

    Article  CAS  PubMed  Google Scholar 

  • Hannaford B, Kim WS, Lee SH, Stark L (1986) Neurological control of head movements: inverse modeling and electromyographic evidence. Math Biosci 78: 159–178

    Article  Google Scholar 

  • Hartwich-Young R, Nelson JS, Sparks DL (1990) The perihypoglossal projection to the superior colliculus in the rhesus monkey. Visual Neurosci 4: 29–42

    Article  CAS  Google Scholar 

  • Kardamakis AA, Moschovakis AK (2006) Implications of interrupted eye-head gaze shifts for resettable integrator reset. Brain Res Bull 70: 171–178

    Article  CAS  PubMed  Google Scholar 

  • Kardamakis A, Moschovakis AK (2009) Optimal control of gaze shifts. J Neurosci 29: 7723–7730

    Article  CAS  PubMed  Google Scholar 

  • Kato R, Grantyn A, Dalezios Y, Moschovakis AK (2006) The local loop of the saccadic system closes downstream of the superior colliculus. Neuroscience 143: 319–337

    Article  CAS  PubMed  Google Scholar 

  • Laurutis VP, Robinson DA (1986) The vestibulo-ocular reflex during human saccadic eye movements. J Physiol 373: 209–233

    CAS  PubMed  Google Scholar 

  • Ling L, Fuchs AF, Phillips JO, Freedman EG (1999) Apparent dissociation between saccadic eye movements and the firing patterns of premotor neurons and motoneurons. J Neurophysiol 82: 2808–2811

    CAS  PubMed  Google Scholar 

  • McCrea RA, Baker R (1985) Anatomical connections of the nucleus prepositus of the cat. J Comp Neurol 237: 377–407

    Article  CAS  PubMed  Google Scholar 

  • McCrea RA, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex in the squirrel monkey. J Comp Neurol 264: 547–570

    Article  CAS  PubMed  Google Scholar 

  • McIlwain JT (1986) Effects of eye position on saccades evoked electrically from the superior colliculus of alert cats. J Neurophysiol 55: 97–112

    CAS  PubMed  Google Scholar 

  • Moschovakis AK (1994) Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. Biol Cybern 70: 291–302

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis AK (1996) Neural network simulations of the primate oculomotor system. II. Frames of reference. Brain Res Bull 40: 337–345

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis AK, Highstein SM (1994) The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 17: 465–488

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis AK, Scudder CA, Highstein SM (1996) The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol 50: 133–254

    Article  CAS  PubMed  Google Scholar 

  • Moschovakis AK, Dalezios Y, Petit J, Grantyn AA (1998a) New mechanism that accounts for position sensitivity of saccades evoked in response to electrical stimulation of superior colliculus. J Neurophysiol 80: 3373–3379

    CAS  PubMed  Google Scholar 

  • Moschovakis AK, Kitama T, Dalezios Y, Petit J, Brandi AM, Grantyn AA (1998b) An anatomical substrate for the spatiotemporal transformation. J Neurosci 18: 10219–10229

    CAS  PubMed  Google Scholar 

  • Moschovakis AK, Kardamakis A, Grantyn A (2008) A new model of primate eye-head gaze shifts. In: Proceedings of the Society for Neuroscience, Washington, p 263.261

  • Pélisson D, Prablanc C, Urquizar C (1988) Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans. J Neurophysiol 59: 997–1013

    PubMed  Google Scholar 

  • Petit J, Klam F, Grantyn A, Berthoz A (1999) Saccades and multisaccadic gaze shifts are gated by different pontine omnipause neurons in head-fixed cats. Exp Brain Res 125: 287–301

    Article  CAS  PubMed  Google Scholar 

  • Phillips JG, Ling L, Fuchs AF, Siebold C, Plorde JJ (1995) Rapid horizontal gaze movement in the monkey. J Neurophysiol 73: 1632–1652

    CAS  PubMed  Google Scholar 

  • Prsa M, Galiana HL (2007) Visual-vestibular interaction hypothesis for the control of orienting gaze shifts by brain stem omnipause neurons. J Neurophysiol 97: 1149–1162

    Article  PubMed  Google Scholar 

  • Pulaski PD, Zee DS, Robinson DA (1981) The behavior of the vestibulo-ocular reflex at high velocities of head rotation. Brain Res 222: 159–165

    Article  CAS  PubMed  Google Scholar 

  • Ramos CF, Stark LW (1987) Simulation studies of descending and reflex control of fast movements. J Mot Behav 19: 38–61

    Google Scholar 

  • Robinson DA (1981) Control of eye movements. In: Brooks VB (eds) The nervous system. Williams and Wilkins, Baltimore, pp 1275–1320

    Google Scholar 

  • Russo GS, Bruce CJ (1993) Effect of eye position within the orbit on electrically elicited saccadic eye movements: A comparison of the macaque monkey’s frontal and supplementary eye fields. J Neurophysiol 69: 800–818

    CAS  PubMed  Google Scholar 

  • Sasaki S (1992) Reticulospinal control of head movements in the cat. In: Berthoz A, Graf W, Vidal P-P. (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 311–317

    Google Scholar 

  • Segraves MA, Goldberg MF (1992) Properties of eye and head movements evoked by electrical stimulation of the monkey superior colliculus. In: Berthoz A, Graf W, Vidal P-P. (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 292–295

    Google Scholar 

  • Sklavos SG, Moschovakis AK (2002) Neural network simulations of the primate oculomotor system. IV. A distributed bilateral stochastic model of the neural Integrator of the vertical saccadic system. Biol Cybern 86: 97–109

    Article  CAS  PubMed  Google Scholar 

  • Sylvestre PA, Cullen KE (2006) Premotor correlates of integrated feedback control for eye-head gaze shifts. J Neurosci 26: 4922–4929

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson RD (1990) Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades. J Neurophysiol 64: 1873–1891

    CAS  PubMed  Google Scholar 

  • Tomlinson RD, Bahra PS (1986) Combined eye-head gaze shifts in the primate. I. Metrics. J Physiol 56: 1542–1557

    CAS  Google Scholar 

  • Tomlinson RD, Bahra PS (1986) Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex. J Physiol 56: 1558–1570

    CAS  Google Scholar 

  • Tomlinson RD, Bance M (1992) Brain stem control of coordinated eye-head gaze shifts. In: Berthoz A, Graf W, Vidal P-P. (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 356–361

    Google Scholar 

  • Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51: 1121–1136

    CAS  PubMed  Google Scholar 

  • van Gisbergen JAM, Robinson DA, Gielen S (1981) A quantitative analysis of generation of sacccadic eye movements by burst neurons. J Neurophysiol 45: 417–442

    PubMed  Google Scholar 

  • Volle M, Guitton D (1993) Human gaze shifts in which head and eyes are not initially aligned. Exp Brain Res 94: 463–470

    Article  CAS  PubMed  Google Scholar 

  • Whittington DA, Lestienne F, Bizzi E (1984) Behavior of preoculomotor burst neurons during eye-head coordination. Exp Brain Res 55: 215–222

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Applied and Computational Mathematics, FORTH, Heraklion, Crete, Greece

    A. A. Kardamakis & A. K. Moschovakis

  2. Department of Basic Sciences, Faculty of Medicine, University of Crete, P.O. Box 2208, 71003, Heraklion, Crete, Greece

    A. A. Kardamakis & A. K. Moschovakis

  3. Lab. de Physiologie de la Perception et de l’Action, College de France, CNRS, Paris, France

    A. Grantyn

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  1. A. A. Kardamakis
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Correspondence to A. K. Moschovakis.

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Kardamakis, A.A., Grantyn, A. & Moschovakis, A.K. Neural network simulations of the primate oculomotor system. V. Eye–head gaze shifts. Biol Cybern 102, 209–225 (2010). https://doi.org/10.1007/s00422-010-0363-0

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