Skip to main content
Log in

Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Rapid gaze shifts are often accomplished with coordinated movements of the eyes and head, the relative amplitude of which depends on the starting position of the eyes. The size of gaze shifts is determined by the superior colliculus (SC) but additional processing in the lower brain stem is needed to determine the relative contributions of eye and head components. Models of eye–head coordination often assume that the strength of the command sent to the head controllers is modified by a signal indicative of the eye position. Evidence in favor of this hypothesis has been recently obtained in a study of phasic electromyographic (EMG) responses to stimulation of the SC in head-restrained monkeys (Corneil et al. in J Neurophysiol 88:2000–2018, 2002b). Bearing in mind that the patterns of eye–head coordination are not the same in all species and because the eye position sensitivity of phasic EMG responses has not been systematically investigated in cats, in the present study we used cats to address this issue. We stimulated electrically the intermediate and deep layers of the caudal SC in alert cats and recorded the EMG responses of neck muscles with horizontal and vertical pulling directions. Our data demonstrate that phasic, short latency EMG responses can be modulated by the eye position such that they increase as the eye occupies more and more eccentric positions in the pulling direction of the muscle tested. However, the influence of the eye position is rather modest, typically accounting for only 10–50% of the variance of EMG response amplitude. Responses evoked from several SC sites were not modulated by the eye position.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4.
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • André-Deshays C, Berthoz A, Revel M (1988) Eye–head coupling in humans. I. Simultaneous recording of isolated motor units in dorsal neck muscles and horizontal eye movements. Exp Brain Res 69:399–406

    Article  PubMed  Google Scholar 

  • Barnes GR (1979) Vestibulo-ocular function during co-ordinated head and eye movements to acquire visual targets. J Physiol Lond 287:127–147

    PubMed  CAS  Google Scholar 

  • Bizzi E, Kalil RE, Tagliasco V (1971) Eye head coordination in monkeys: evidence for centrally patterned organization. Sci Wash D C 173:452–454

    Article  Google Scholar 

  • Blakemore C, Donaghy M (1980) Coordination of head and eyes in the gaze changing behaviour of cats. J Physiol Lond 300:317–335

    PubMed  CAS  Google Scholar 

  • Brinkworth RS, Turker KS (2003) A method for quantifying reflex responses from intra-muscular and surface electromyogram. J Neurosci Methods 122:179–193

    Article  PubMed  Google Scholar 

  • Collewijn H (1977) Eye and head movements in freely moving rabbits. J Physiol Lond 266:471–498

    PubMed  CAS  Google Scholar 

  • Corneil BD, Olivier E, Richmond FJR, Loeb GE, Munoz DP (2001) Neck muscles of the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. J Neurophysiol 86:1729–1749

    PubMed  CAS  Google Scholar 

  • 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 88:1980–1999

    Google Scholar 

  • Corneil BD, Olivier E, Munoz DP (2002b) Neck muscle responses to stimulation of monkey superior colliculus. II. Gaze shift initiation and volitional head movement. J Neurophysiol 88:2000–2018

    Google Scholar 

  • Cowie RJ, Robinson DL (1994) Subcortical contributions to head movements in macaques: I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus. J Neurophysiol 72:2648–2664

    PubMed  CAS  Google Scholar 

  • Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol 45:302–304

    Article  PubMed  CAS  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  Google Scholar 

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

    CAS  Google Scholar 

  • 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 76:927–952

    PubMed  CAS  Google Scholar 

  • Fuller JH (1992) Head movement propensity. Exp Brain Res 92:152–164

    Article  PubMed  CAS  Google Scholar 

  • Grantyn A, Berthoz A (1985) Burst activity of identified tectoreticulo-spinal neurons in the alert cat. Exp Brain Res 57:417–421

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting to the tecto-bulbo-spinal tract. Exp Brain Res 46:243–256

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gresty MA (1974) Coordination of head and eye movements to fixate continuous and intermittent targets. Vision Res 14:395–403

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Isa T, Naito K (1994) Activity of neurons in Forel’s field H during orienting head movements in alert head-free cats. Exp Brain Res 100:187–199

    Article  PubMed  CAS  Google Scholar 

  • Isa T, Naito K (1995) Activity of neurons in the medial pontomedullary reticular formation during orienting movements in alert head-free cats. J Neurophysiol 74:73–95

    PubMed  CAS  Google Scholar 

  • Isa T, Itouji T, Sasaki S (1988) Excitatory pathways from Forel’s field H to head elevator motoneurones in the cat. Neurosci Lett 90:89–94

    Article  PubMed  CAS  Google Scholar 

  • Keshner EA, Baker JF, Banovetz J, Peterson BW (1992) Patterns of neck muscle activation in cats during reflex and voluntary head movements. Exp Brain Res 88:361–374

    Article  PubMed  CAS  Google Scholar 

  • Kitama T, Grantyn A, Berthoz A (1995) Orienting related eye–neck neurons of the medial ponto-bulbar reticular formation do not participate in horizontal canal-dependent vestibular reflexes of alert cats. Brain Res Bull 38:337–347

    Article  PubMed  CAS  Google Scholar 

  • Kokkoroyannis T, Scudder CA, Highstein SM, Balaban C, Moschovakis AK (1996) The anatomy and physiology of the primate Interstitial Nucleus of Cajal. I. Efferent projections. J Neurophysiol 75:725–739

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lestienne F, Vidal P-P, Berthoz A (1984) Gaze changing behavior in head restrained monkey. Exp Brain Res 53:349–356

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Moschovakis AK (1997) The neural integrators of the mammalian saccadic system. Front Biosci 2:552–577

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munoz DP, Guitton D, Pelisson D (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 66:1642–1666

    PubMed  CAS  Google Scholar 

  • Olivier E, Grantyn A, Kitama T, Berthoz A (1995) Post-spike facilitation of neck EMG by cat tectoreticulospinal neurones during orienting movements. J Physiol 482:455–466

    PubMed  CAS  Google Scholar 

  • Paré M, Crommelinck M, Guitton D (1994) Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity. Exp Brain Res 101:123–139

    PubMed  Google Scholar 

  • Pelisson 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 41:25–26

    Article  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

    PubMed  CAS  Google Scholar 

  • Richmond FJR, Thomson DB, Loeb GE (1992) Electromyographic studies of neck muscles in the intact cat. I. Patterns of recruitment underlying posture and movement during natural behaviors. Exp Brain Res 88:41–58

    Article  PubMed  CAS  Google Scholar 

  • Roucoux A, Crommelinck M (1988) Control of head movement during visual orientation. In: Peterson BW, Richmond FJ (eds) Control of head movement. Oxford University Press, New York, pp 208–223

    Google Scholar 

  • Roucoux A, Vidal PP, Veraart C, Crommelinck M, Berthoz A (1982) The relation of neck muscles activity to horizontal eye position in the alert cat. I. Head fixed. In: Crommelinck ARaM (ed) Physiological and pathological aspects of eye movements. W. Junk, The Hague

    Google Scholar 

  • Roucoux A, Crommelinck M, Decostre M-F (1989) Neck muscle activity in eye–head coordinated movements. In: Hulliger JHJAaM (ed) Progress in brain research, vol 80. Elsevier, Amsterdam, pp 351–362

  • Stahl JS (1999) Amplitude of human head movements associated with horizontal saccades. Exp Brain Res 126:41–54

    Article  PubMed  CAS  Google Scholar 

  • Thomson DB, Loeb GE, Richmond FJR (1996) Effect of neck posture on patterns of feline neck muscles during horizontal rotation. Exp Brain Res 110:392–400

    Article  PubMed  CAS  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 

  • Vidal P-P, Roucoux A, Berthoz A (1982) Horizontal eye position related activity in neck muscles of the alert cat. Exp Brain Res 46:448–453

    Article  PubMed  CAS  Google Scholar 

  • Wickland CR, Baker JF, Peterson BW (1991) Torque vectors of neck muscles. Exp Brain Res 84:649–659

    Article  PubMed  CAS  Google Scholar 

  • Zangemeister WH, Stark L (1982) Types of gaze movement: variable interactions of eye and head movements. Exp Neurol 77:563–577

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the financial support from the French Ministry of Research (Grant ACI 2003 N°03 5 45).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. K. Moschovakis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hadjidimitrakis, K., Moschovakis, A.K., Dalezios, Y. et al. 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 (2007). https://doi.org/10.1007/s00221-006-0765-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0765-3

Keywords

Navigation