Summary
A tonic coupling between the horizontal component of eye position and dorsal neck muscle activity has been demonstrated in animals and humans. In addition, a transient saccade related coupling has been found in animals. In order to investigate such a phasic component of the eye-head synergy in humans, we have recorded the activity of isolated motor units in the splenius muscle during large horizontal eye movements in head fixed subjects. Eye movement recording was achieved by conventional binocular electro-oculography and the activity of the right splenius muscle was recorded with Bronks coaxial electrodes inserted manually at the C4–C5 intervertebral level. We found two main types of motor unit discharge patterns in the splenius (SPMU), the first type (type A, 14 SPMUs) shows a phasic modulation of firing rate during saccades with a triphasic profile composed of a pre-saccadic suppression, a per-saccadic burst and a post saccadic tonic discharge proportional to eye position. The second type (type B, 6 SPMUs) exhibits little, if any, modulation of firing rate with either fixation or saccades. These results suggest that eye-head coupling is present not only during the fixation period but also during saccades and that a phasic activity or suppression related to saccadic eye velocity is present in dorsal neck muscle EMG.
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References
Abrahams VC, Rose PK (1975) Projections of extraocular, neck muscles and retinal afferents to superior colliculus in the cat: their connections to cells of origin of tectospinal tract. J Neurophysiol 38: 10–18
Anderson ME (1977) Segmental reflex inputs to motoneurons in nervating dorsal neck musculature in the cat. Exp Brain Res 28: 175–187
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
Basmajian JV, De Luca CJ (1985) Control properties of motor units. In: Williams J, Wilkins J (eds) Muscles alive: their functions revealed by electromyography, 5 edn. Baltimore, London, Sydney, pp 125–167
Berthoz A, Vidal PP, Corvisier J (1982) Brainstem neurons mediating horizontal eye position signals to the dorsal neck muscles. In: Roucoux A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. Dr. Junk Publ, The Hague, pp 383–398
Berthoz A, Grantyn A (1985) Neuronal mechanisms underlying eye-head coordination. Progr Brain Res 6: 1–19
Berthoz A, Droulez J, Vidal PP, Yoshida K (1989) Neural correlates of horizontal vestibulo-ocular cancellation during rapid eye movements in the cat. J Physiol Lond 419: 717–751
Bizzi E, Kalil RE, Tagliasco V (1971) Eye-head coordination in monkeys: evidence for centrally patterned organization. Science 173: 452–454
Conrad B, Benecke R, Goehmann M (1983) Premovement silent period in fast movement initiation. Exp Brain Res 51: 310–313
Coulter JD, Bowker RM, Wise SP, Murray EA, Castiglioni AJ, Westlund KN (1979) Cortical, tectal and medullary descending pathways to the cervical spinal cord. Progr Brain Res 50: 263–274
Delgado-Garcia JM, Del Pozo F, Baker R (1986) Behavior of neurons in the abducens nucleus of the alert cat. I. Motoneurons. Neuroscience 17: 929–952
Fuchs AF, Kaneko CRS, Scudder CA (1985) Brainstem control of saccadic eye movements. Ann Rev Neurosci 8: 307–337
Fuller JH (1980) Linkage of eye and head movements in the alert rabbit. Brain Res 205: 363–381
Grantyn A, Berthoz A (1985) Burst activity of identified tectoreticulo-spinal neurons in the alert cat. Exp Brain Res 57: 417–421
Grantyn A, Berthoz A (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioural properties. Exp Brain Res 66: 458–474
Grantyn A, Hardy O, Berthoz A (1990) Control of visually triggered orienting eye and head movements by cooperative action of tecto and reticulospinal neurons. In: Berthoz A, Graf W, Vidal PP (eds) The head neck sensory-motor system. Oxford University Press, New York (in press)
Guitton D, Douglas RM, Volle M (1984) Eye-head coordination in cats. J Neurophysiol 52: 1030–1050
Henn V, Cohen B (1973) Quantitative analysis of activity in eye muscle motoneurons during saccadic eye movements and positions of fixation. J Neurophysiol 1: 115–126
Keschner EA, Campbell D, Katz RT, Peterson BW (1989) Neck muscle activation pattern in humans during isometric head stabilization. Exp Brain Res 75: 335–344
Lestienne F, Vidal PP, Berthoz A (1984) Gaze changing behaviour in head restrained monkey. Exp Brain Res 53: 349–356
Mayoux-Benhamou MA, Wybier M, Revel (1990) CT scan study of the muscles of the neck in man. Method of insertion of wire electrodes. In: Berthoz A, Graf W, Vidal PP (eds) The head-neck sensory motor system. Oxford University Press, New York (in press)
Nardone A, Schieppati M (1988) Postural adjustements associated with voluntary contraction of leg muscles in standing man. Exp Brain Res 69: 469–481
Peterson BW, Fukushima K (1982) The reticulo-spinal system and its role in generating vestibular and visuo-motor reflexes. In: Sjoklund R, Björklund A (eds) Brainstem control of spinal mechanisms. Elsevier, North Holland Amsterdam, pp 225–229
Richmond FJR, Abrahams VC (1975) Morphology and enzyme histochemistry of dorsal neck muscles in the cat neck. J Neurophysiol 32: 1312–1322
Roucoux A, Vidal PP, Veraart C, Crommelinck M, Berthoz A (1982) The relation of neck muscle activity to horizontal eye position in the alert cat I. Head fixed. In: Roucoux A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. Junk, The Hague Boston London, pp 371–378
Roucoux A, Crommelinck M, Decostre MF (1989) Neck muscle activity in eye-head coordinated movements. Progr Brain Res 80: 351–362
Sazaki S, Shimazu H (1981) Reticulo-vestibular organization participating in generation of horizontal fast eye movements. Ann N Y Acad Sci 374: 130–143
Sazaki S (1990) Reticulo-spinal control of head movements in the cat. In: Berthoz A, Graf W, Vidal PP (eds) The head neck sensory motor system. Oxford University Press, New York (in press)
Sindermann F, Geiselmann B, Fischler M (1978) Single motor unit activity in extraocular muscles during fixation and saccades. EEG Clin Neurophys 45: 64–73
Stark L, Zangeimester WH, Hannaford B (1988) Movements models, optimal control theory and clinical application. In: Peterson BW Richmonds FJ (eds) Control of head movement. Oxford University Press, New York, pp 243–250
Takebe K, Vitti M, Basmajian JV (1974) The functions of semispinalis capitis and splenius capitis muscles: an electromyographic study. Anat Rec 179: 477–480
Tokizane T and Shimazu H (1964) Functional differentiation of human skeletal muscle: corticalization and spinalization of movements. Thomas, Springfield IL, p 60
Uchino Y, Hiraï N, Suzuki S (1982) Branching pattern and properties of vertical and horizontal-related excitatory vestibulo-ocular neurons in the cat. J Neurophysiol 48: 891–903
Vidal PP, Roucoux A, Berthoz A (1982) Horizontal eye position related activity in neck muscles of the alert cat. Exp Brain Res 46: 448–453
Vidal PP, Corvisier J, Berthoz A (1983) Eye and neck motor signals in periabducens reticular neurons of the alert cat. Exp Brain Res 53: 16–28
Vidal PP, Graf W, Berthoz A (1986) The orientation of the cervical vertebral column in unrestrained awake animals. I. Resting position. Exp Brain Res 61: 549–559
Zangemeister WH, Stark L (1982) Types of gaze movement: variable interaction of eye and head movements. Exp Neurol 77: 563–577
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André-Deshays, C., Revel, M. & Berthoz, A. Eye-head coupling in humans. Exp Brain Res 84, 359–366 (1991). https://doi.org/10.1007/BF00231457
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DOI: https://doi.org/10.1007/BF00231457