Saccade-related, long-lead burst neurons in the monkey rostral pons.

The paramedian pontine reticular formation contains the premotoneuronal cell groups that constitute the saccadic burst generator and control saccadic eye movements. Despite years of study and numerous investigations, the rostral portion of this area has received comparatively little attention, particularly the cell type known as long-lead burst neurons (LLBNs). Several hypotheses about the functional role of LLBNs in saccade generation have been proposed, although there is little information with which to assess them. To address this issue, I mapped and recorded LLBNs in the rostral pons to measure their discharge characteristics and correlate those characteristics with the metrics of the concurrent saccades. On the basis of their discharge and location, I identified three types of LLBNs in the rostral pons: excitatory (eLLBN), dorsal (dLLBN), and nucleus reticularis tegmenti pontis (nrtp) LLBNs. The eLLBNs, encountered throughout the pons, discharge for ipsilateral saccades in proportion to saccade amplitude, velocity, and duration. The dLLBNs, found at the pontomesencephalic junction, discharge maximally for ipsilateral saccades of a particular amplitude, usually <10 degrees , and are not associated with a particular anatomical nucleus. The nrtp LLBNs, previously described as vector LLBNs, discharge for saccades of a particular direction and sometimes a particular amplitude. The discharge of the eLLBNs suggests they drive motor neurons. The anatomical projections of the nrtp LLBNs suggest that their involvement in saccade production is less direct. The discharge of dLLBNs is consistent with a role in providing the "trigger" signal that initiates saccades.

[1]  M. Yamashita,et al.  Inhibitory input to pause neurons from pontine burst neuron area in the cat , 1996, Neuroscience Letters.

[2]  A. Fuchs,et al.  Role of cat pontine burst neurons in generation of saccadic eye movements. , 1981, Journal of neurophysiology.

[3]  L. Optican,et al.  Model of the control of saccades by superior colliculus and cerebellum. , 1999, Journal of neurophysiology.

[4]  A. Fuchs,et al.  Afferents to the abducens nucleus in the monkey and cat , 1986, The Journal of comparative neurology.

[5]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. , 1986, The Journal of comparative neurology.

[6]  C. Kaneko,et al.  Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys II. Pursuit, vestibular, and optokinetic responses. , 1999, Journal of neurophysiology.

[7]  Y. Shinoda,et al.  Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat. , 1999, Journal of neurophysiology.

[8]  C. K. Henkel,et al.  Superior colliculus connections with the extraocular motor nuclei in the cat , 1978, The Journal of comparative neurology.

[9]  M. Goldberg,et al.  Effect of short-term saccadic adaptation on saccades evoked by electrical stimulation in the primate superior colliculus. , 2002, Journal of neurophysiology.

[10]  K. Hepp,et al.  Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF) , 2004, Experimental Brain Research.

[11]  A K Moschovakis,et al.  Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons. , 1996, Journal of neurophysiology.

[12]  A. Fuchs,et al.  Evidence against a moving hill in the superior colliculus during saccadic eye movements in the monkey. , 2002, Journal of neurophysiology.

[13]  C. Kaneko Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. , 1996, Journal of neurophysiology.

[14]  D. Munoz,et al.  Gaze control in the cat: studies and modeling of the coupling between orienting eye and head movements in different behavioral tasks. , 1990, Journal of neurophysiology.

[15]  H Shimazu,et al.  Monosynaptic activation of medium-lead burst neurons from the superior colliculus in the alert cat. , 1996, Journal of neurophysiology.

[16]  T. Kitama,et al.  Characteristics of Medullary Neurons That Drive Bursters for Horizontal Rapid Eye Movements in the Alert Cat , 1992 .

[17]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[18]  C. Scudder,et al.  The microscopic anatomy and physiology of the mammalian saccadic system , 1996, Progress in Neurobiology.

[19]  O. Hikosaka,et al.  Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey , 1996, Experimental Brain Research.

[20]  A. Fuchs,et al.  Brainstem control of saccadic eye movements. , 1985, Annual review of neuroscience.

[21]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[22]  C. Kaneko,et al.  Brainstem afferents to the oculomotor omnipause neurons in monkey , 1990, The Journal of comparative neurology.

[23]  D. Sparks Functional properties of neurons in the monkey superior colliculus: Coupling of neuronal activity and saccade onset , 1978, Brain Research.

[24]  D L Sparks,et al.  Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades. , 1993, Journal of neurophysiology.

[25]  W. Becker,et al.  An analysis of the saccadic system by means of double step stimuli , 1979, Vision Research.

[26]  Robert M. McPeek,et al.  Evidence against direct connections to PPRF EBNs from SC in the monkey. , 2000, Journal of neurophysiology.

[27]  H Shimazu,et al.  Vestibular and Visual Interaction in Generation of Rapid Eye Movements a , 1992, Annals of the New York Academy of Sciences.

[28]  A. Fuchs,et al.  Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. , 2002, Journal of neurophysiology.

[29]  K. Fukushima,et al.  Discharge characteristics of vestibular saccade neurons in alert monkeys. , 1998, Journal of neurophysiology.

[30]  A. Fuchs,et al.  Activity of brain stem neurons during eye movements of alert monkeys. , 1972, Journal of neurophysiology.

[31]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[32]  A. Fuchs,et al.  Oblique saccadic eye movements of the cat , 2004, Experimental Brain Research.

[33]  Christian Quaia,et al.  Distributed model of control of saccades by superior colliculus and cerebellum , 1998, Neural Networks.

[34]  O. Hikosaka,et al.  Inhibitory reticular neurons related to the quick phase of vestibular nystagmus — Their location and projection , 1977, Experimental Brain Research.

[35]  A. Fuchs,et al.  Discharge of monkey nucleus reticularis tegmenti pontis neurons changes during saccade adaptation. , 2005, Journal of neurophysiology.

[36]  Division on Earth Guide for the Care and Use of Laboratory Animals , 1996 .

[37]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[38]  David L. Sparks,et al.  Systematic errors for saccades to remembered targets: Evidence for a dissociation between saccade metrics and activity in the superior colliculus , 1994, Vision Research.

[39]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons , 1986, The Journal of comparative neurology.

[40]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

[41]  B. Cohen,et al.  Coding of information about rapid eye movements in the pontine reticular formation of alert monkeys , 1976, Brain Research.

[42]  E. Keller,et al.  Colliculoreticular organization in primate oculomotor system. , 1977, Journal of neurophysiology.

[43]  J. Schlag,et al.  Illusory localization of stimuli flashed in the dark before saccades , 1995, Vision Research.

[44]  N J Gandhi,et al.  Discharge of superior collicular neurons during saccades made to moving targets. , 1996, Journal of neurophysiology.

[45]  A Berthoz,et al.  Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. , 1982, Journal of neurophysiology.

[46]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. , 1993, Journal of neurophysiology.

[47]  R H Wurtz,et al.  Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus. , 1982, Journal of neurophysiology.

[48]  T. Vilis,et al.  Characteristics of saccadic dysmetria in monkeys during reversible lesions of medial cerebellar nuclei. , 1981, Journal of neurophysiology.

[49]  T. Kitama,et al.  An Anatomical Substrate for the Spatiotemporal Transformation , 1998, The Journal of Neuroscience.

[50]  A. Fuchs,et al.  The brainstem burst generator for saccadic eye movements , 2002, Experimental Brain Research.

[51]  C. Kaneko,et al.  Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. I. Saccades and fixation. , 1997, Journal of neurophysiology.

[52]  H Shimazu,et al.  Site of interaction between saccade signals and vestibular signals induced by head rotation in the alert cat: functional properties and afferent organization of burster-driving neurons. , 1995, Journal of neurophysiology.

[53]  A. Fuchs,et al.  Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. , 1979, Journal of neurophysiology.

[54]  Kaoru Yoshida,et al.  Saccade-related inhibitory input to pontine omnipause neurons: an intracellular study in alert cats. , 1999, Journal of neurophysiology.

[55]  C. Scudder A new local feedback model of the saccadic burst generator. , 1988, Journal of neurophysiology.

[56]  A. Fuchs,et al.  The neuronal substrate of integration in the oculomotor system , 1992, Progress in Neurobiology.

[57]  A. Fuchs,et al.  Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. , 1988, Journal of neurophysiology.

[58]  Neeraj J Gandhi,et al.  Effects of partial lidocaine inactivation of the paramedian pontine reticular formation on saccades of macaques. , 2003, Journal of neurophysiology.

[59]  E. Keller,et al.  Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. , 1985, Journal of neurophysiology.

[60]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.