Abstract
Constant frequency microstimulation of the paramedian pontine reticular formation (PPRF) in head-restrained monkeys evokes a constant velocity eye movement. Since the PPRF receives significant projections from structures that control coordinated eye-head movements, we asked whether stimulation of the pontine reticular formation in the head-unrestrained animal generates a combined eye-head movement or only an eye movement. Microstimulation of most sites yielded a constant-velocity gaze shift executed as a coordinated eye-head movement, although eye-only movements were evoked from some sites. The eye and head contributions to the stimulation-evoked movements varied across stimulation sites and were drastically different from the lawful relationship observed for visually-guided gaze shifts. These results indicate that the microstimulation activated elements that issued movement commands to the extraocular and, for most sites, neck motoneurons. In addition, the stimulation-evoked changes in gaze were similar in the head-restrained and head-unrestrained conditions despite the assortment of eye and head contributions, suggesting that the vestibulo-ocular reflex (VOR) gain must be near unity during the coordinated eye-head movements evoked by stimulation of the PPRF. These findings contrast the attenuation of VOR gain associated with visually-guided gaze shifts and suggest that the vestibulo-ocular pathway processes volitional and PPRF stimulation-evoked gaze shifts differently.








Similar content being viewed by others
References
Andre-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
Breznen B, Lu SM, Gnadt JW (1996) Analysis of the step response of the saccadic feedback: system behavior. Exp Brain Res 111:337–344
Chen LL, Walton MM (2005) Head movement evoked by electrical stimulation in the supplementary eye field of the rhesus monkey. J Neurophysiol 94:4502–4519
Cohen B, Komatsuzaki A (1972) Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp Neurol 36:101–117
Corneil BD, Olivier E, Munoz DP (2002) Neck muscle activity evoked by stimulation of the monkey superior colliculus. I. Topography and manipulation of stimulation parameters. J Neurophysiol 88:1980–1999
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
Cowie RJ, Smith MK, Robinson DL (1994) Subcortical contributions to head movements in macaques. II. Connections of a medial pontomedullary head-movement region. J Neurophysiol 72:2665–2682
Cullen KE, Guitton D (1997) Analysis of primate IBN spike trains using system identification techniques. II. Relationship to gaze, eye, and head movement dynamics during head-free gaze shifts. J Neurophysiol 78:3283–3306
Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933
Cullen KE, Huterer M, Braidwood DA, Sylvestre PA (2004) Time course of vestibuloocular reflex suppression during gaze shifts. J Neurophysiol 92:3408–3422
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
Freedman EG, Sparks DL (1997b) Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77:2328–2348
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
Gandhi NJ, Sparks DL (2000) Microstimulation of the pontine reticular formation in monkey: effects on coordinated eye-head movements. Soc Neurosci Abstr 109.8
Gandhi NJ, Sparks DL (2001) Experimental control of eye and head positions prior to head-unrestrained gaze shifts in monkey. Vision Res 41:3243–3254
Gandhi NJ, Sparks DL (2007) Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region. J Neurophysiol 98:360–373
Grantyn A, Berthoz A (1987) Reticulo-spinal 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
Grantyn A, Berthoz A (1988) The role of the tectoreticulospinal system in the control of head movement. In: Peterson BW, Richmond FJ (eds) Control of head movement. Oxford University Press, New York, pp 224–244
Grantyn A, Ong-Meang Jacques V, Berthoz A (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Exp Brain Res 66:355–377
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
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
Huerta MF, Harting JK (1982) Tectal control of spinal cord activity: neuroanatomical demonstration of pathways connecting the superior colliculus with the cervical spinal cord grey. Prog Brain Res 57:293–328
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
Iwamoto Y, Sasaki S (1990) Monosynaptic excitatory connections of reticulospinal neurones in the nucleus reticularis pontis caudalis with dorsal neck motoneurones in the cat. Exp Brain Res 80:277–289
Iwamoto Y, Sasaki S, Suzuki I (1990) Input-output organization of reticulospinal neurones, with special reference to connections with dorsal neck motoneurones in the cat. Exp Brain Res 80:260–276
Keller EL (1974) Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37:316–332
Klier EM, Wang H, Crawford JD (2001) The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4:627–632
Knight TA, Fuchs AF (2007) Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation. J Neurophysiol 97:618–634
Laurutis VP, Robinson DA (1986) The vestibulo-ocular reflex during human saccadic eye movements. J Physiol Lond 373:209–233
Lefèvre P, Bottemanne I, Roucoux A (1992) Experimental study and modeling of vestibulo-ocular reflex modulation during large shifts of gaze in humans. Exp Brain Res 91:496–508
Leigh RJ, Zee DS (1999) The neurology of eye movements. Oxford University Press, New York
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
Martinez-Trujillo JC, Wang H, Crawford DJ (2003) Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts. J Neurophysiol 89:2961–2974
May PJ, Porter JD (1992) The laminar distribution of macaque tectobulbar and tectospinal neurons. Vis Neurosci 8:257–276
Missal M, Lefèvre P, Delinte A, Crommelinck M, Roucoux A (1996) Smooth eye movements evoked by electrical stimulation of the cat’s superior colliculus. Exp Brain Res 107:382–390
Miyashita N, Hikosaka O (1996) Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey. Exp Brain Res 112:187–196
Moschovakis AK, Dalezios Y, Petit J, Grantyn AA (1998) New mechanism that accounts for position sensitivity of saccades evoked in response to stimulation of superior colliculus. J Neurophysiol 80:3373–3379
Munoz DP, Guitton D, Pélisson 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
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
Pélisson D, Prablanc C (1986) Vestibulo-ocular reflex (VOR) induced by passive head rotation and goal-directed saccadic eye movements do not simply add in man. Brain Res 380:397–400
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
Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and branching of reticulospinal neurons. Exp Brain Res 23:333–351
Phillips JO, Ling L, Fuchs AF (2001) A comparison of excitatory and inhibitory burst neuron activity during active head-unrestrained gaze shifts. Soc Neurosci Abstr 405.10
Quessy S, Freedman EG (2004) Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis. I. Characteristics of evoked head movements. Exp Brain Res 156:342–356
Reinhart RJ, Zuber BL (1970) Horizontal eye movements from abducens nerve stimulation in the cat. IEEE Trans Biomed Eng 17:11–14
Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808
Robinson FR, Phillips JO, Fuchs AF (1994) Coordination of gaze shifts in primates: brainstem inputs to neck and extraocular motoneuron pools. J Comp Neurol 346:43–62
Roucoux A, Guitton D, Crommelinck M (1980) Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp Brain Res 39:75–85
Roy JE, Cullen KE (1998) A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nat Neurosci 1:404–410
Roy JE, Cullen KE (2002) Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87:2337–2357
Sasaki S, Yoshimura K, Naito K (2004) The neural control of orienting: role of multiple-branching reticulospinal neurons. Prog Brain Res 143:383–389
Schiller PH (1970) The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey. Exp Brain Res 10:347–362
Schiller PH, Stryker M (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35:915–924
Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM (1996) Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons. J Neurophysiol 76:353–370
Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements: A modern synthesis. Exp Brain Res 142:439–462
Sklavos SG, Gandhi NJ, Sparks DL, Porrill J, Dean P (2002) Mechanics of oculomotor plant estimated from effects of abducens microstimulation. Soc Neurosci Abstr 463.5
Sparks DL (1999) Conceptual issues related to the role of the superior colliculus in the control of gaze. Curr Opin Neurobiol 9:698–707
Sparks DL (2002) The brainstem control of saccadic eye movements. Nat Rev Neurosci 3:952–964
Sparks DL, Gandhi NJ (2003) Single cell signals: an oculomotor perspective. Prog Brain Res 142:35–53
Sparks DL, Freedman EG, Chen LL, Gandhi NJ (2001) Cortical and subcortical contributions to coordinated eye and head movements. Vision Res 41:3295–3305
Sprague JM, Chambers WW (1954) Control of posture by reticular formation and cerebellum in the intact, anesthetized and unanesthetized and in the decerebrated cat. Am J Physiol 176:52–64
Stanford TR, Freedman EG, Sparks DL (1996) Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J Neurophysiol 76:3360–3381
Strassman A, Highstein SM, McCrea RA (1986) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 249:337–357
Sylvestre PA, Cullen KE (2006) Premotor correlates of integrated feedback control for eye-head gaze shifts. J Neurosci 26:4922–4929
Tabak S, Smeets JB, Collewijn H (1996) Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head. J Neurophysiol 76:3249–3263
Tohyama M, Sakai K, Salvert D, Touret M, Jouvet M (1979) Spinal projections from the lower brain stem in the cat as demonstrated by the horseradish peroxidase technique. I. Origins of the reticulospinal tracts and their funicular trajectories. Brain Res 173:383–403
Tomlinson RD, Bahra PS (1986) Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex. J Neurophysiol 56:1558–1570
Tu TA, Keating EG (2000) Electrical stimulation of the frontal eye field in a monkey produces combined eye and head movements. J Neurophysiol 84:1103–1106
Van Gisbergen JA, Robinson DA, Gielen S (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 45:417–442
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
Wang X, Zhang M, Cohen IS, Goldberg ME (2007) The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nat Neurosci 10:640–646
Warren S, Waitzman DM, May PJ (2008) Anatomical evidence for interconnections between the central mesencephalic reticular formation and cervical spinal cord in the cat and macaque. Anat Rec 291:141–160
Whittington DA, Lestienne F, Bizzi E (1984) Behavior of preoculomotor burst neurons during eye-head coordination. Exp Brain Res 55:215–222
Zar JH (1999) Biostatistical analysis. Prentice-Hall, Upper Saddle River, NJ
Acknowledgments
We thank Dennis Murray for surgical assistance and animal care, and Kathy Pearson for software development. The study was funded by NIH grants EY001189, EY007001, EY007009 and EY015485.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gandhi, N.J., Barton, E.J. & Sparks, D.L. Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation. Exp Brain Res 189, 35–47 (2008). https://doi.org/10.1007/s00221-008-1401-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-008-1401-1