Anatomical substrates of oculomotor control

Current Opinion in Neurobiology

Volumn 7, Issue 6, 1997, Pages 872-879

  Büttner Ennever, Jean A ^a   Horn, Anja K E ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EYE MOVEMENT; EYE MOVEMENT CONTROL; NEUROANATOMY; OPTOKINETIC STIMULATION; PONS RETICULAR FORMATION; PRIORITY JOURNAL; REVIEW; SACCADIC EYE MOVEMENT; SMOOTH PURSUIT EYE MOVEMENT; VESTIBULOOCULAR REFLEX; VISUAL FIELD;

EID: 0345019799     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(97)80149-3     Document Type: Article

References (66)

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14. Kaneko CRS: Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in Rhesus macaques. J Neurophysiol 1996, 75:2229-2242. A chemical lesion study with careful histological controls demonstrating a decrease in peak saccadic velocity and increase in saccade duration, but no impairment of fixation, after damage of the omnipause neurons.
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17. Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM: Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons. J Neurophysiol 1996, 76:353-370. This is the first detailed description of the projection targets of physiologically identified saccadic long-lead burst neurons (LLBNs) in the pontine reticular formation using intra-axonal HRP-injections in the primate. Three types of LLBNs were reconstructed: precerebellar LLBNs in the nucleus reticularis tegmenti pontis (nrtp), reticulo-spinal LLBNs in the excitatory burst neuron (EBN) area and pontine LLBNs in the nucleus reticularis pontis oralis with projections to the EBN and omnipause neuron area. The combination of detailed anatomy and physiology in this type of study is invaluable for further progress in understanding the brainstem control of saccades.
18. Waitzman DM, Silakov VL, Cohen B: Central mesencephalic reticular formation (cMRF) neurons discharging before and during eye movements. J Neurophysiol 1996, 75:1546-1572. A physiological characterisation of neurons in the cMRF suggesting an important role in saccades, providing the superior colliculus with information on the current eye displacement during a saccade.
19. Kamogawa H, Ohki Y, Shimazu H, Suzuki I, Yamashita M: Inhibitory input to pause neurons from pontine burst neuron area in the cat Neurosci Lett 1996, 203:163-166. A specific area of nucleus reticularis pontis caudalis within the excitatory burst neuron area, purported to contain long-lead burst neurons, was found to be the most effective site from which omnipause neurons could be inhibited by electrical stimulation.
20. Munoz DP, Waitzman DM, Wurtz RH: Activity of neurons in monkey superior colliculus during interrupted saccades. J Neurophysiol 1996, 75:2562-2580. A stimulation and recording study in the superior colliculus (SC) of monkey suggesting that fixation cells in the rostral SC inhibit burst and build-up neurons in the caudal SC.
21. Chimoto S, Iwamoto Y, Shimazu H, Yoshida K: Functional connectivity of the superior colliculus with saccade-related brain stem neurons in the cat Prog Brain Res 1996, 112:157-165. An electrophysiological study in the cat showing that stimulation of the caudal superior colliculus (SC) activates premotor burst neurons at monosynaptic latencies, which do not respond to stimulation of the rostral SC. Stimulation of the rostral SC activates omnipause neurons directly, which are inhibited after stimulation of the caudal SC.
22. Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM: Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon. J Neurophysiol 1996, 76:332-352. An excellent intracellular-HRP-injection study of physiologically identified mesencephalic long-lead burst neurons showing for the first time the projection targets within the paramedian pontine reticular formation.
23. Sato A, Ohtsuka K: Projection from the accommodation-related area in the superior colliculus of the cat. J Comp Neurol 1996, 367:465-476. An interesting physiological-anatomical study of superior colliculus efferents. However, the authors' location of the nucleus raphe interpositus (rip) is incorrect.
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26. Missal M, Lefevre P, Delinte A, Crommelinck M, Roucoux A: Smooth eye movements evoked by electrical stimulation of the cat's superior colliculus. Exp Brain Res 1996, 107:382-390. Another study about slow eye movements after stimulation of the superior colliculus (see [23•]) examining the effects of stimulation parameters upon movement velocity.
27. Breznen B, Lu SM, Gnadt JW: Analysis of the step response of the saccadic feedback system: behavior. Exp Brain Res 1996, 111:337-344. This paper proposes an alternative hypothesis for the generation of slow eye movements after prolonged stimulation of the superior colliculus.
28. Schwarz C, Thier P: Comparison of projection neurons in the pontine nuclei and the nucleus reticularis tegmenti pontis of the rat. J Comp Neurol 1996, 376:403-419. A useful double-labelling technique for studying the detailed morphology of retrogradely identified neurons, and applied here to an area of high interest.
29. Gamlin PDR, Clarke RJ: Single-unit activity in the primate nucleus reticularis tegmenti pontis related to vergence and ocular accommodation. J Neurophysiol 1995, 73:2115-2119.
30. Averbuch Heller L, Leigh RJ: Eye movements. Curr Opin Neurol 1996, 9:26-31.
31. Yamada T, Suzuki DA, Yee RD: Smooth pursuit-like eye movements evoked by microstimulation in macaque nucleus reticularis tegmenti pontis. J Neurophysiol 1996, 76:3313-3324. The exact reconstruction of stimulation sites reveal a topography in nrtp in which a new smooth-pursuit-like area lies rostromedially and the saccade-like neurons lie in caudal nrtp.
32. Van Opstal AJ, Hepp K, Suzuki Y, Henn V: Role of monkey nucleus reticularis tegmenti pontis in stabilization of Listing's plane. J Neurosci 1997, 16:7284-7296. This study provides evidence for neural circuits implementing Listing's law, rather than passive orbital forces - a controversial topic.
33. Fukushima K, Kaneko CRS, Fuchs AF: The neuronal substrate of integration in the oculomotor system. Prog Neurobiol 1992, 39:609-639.
34. Kokkoroyannis T, Scudder CA, Balaban CD, Highstein SM, Moschovakis AK: Anatomy and physiology of the primate interstitial nucleus of Cajal. 1. Efferent projections. J Neurophysiol 1996, 75:725-739. This is the first anatomical description of efferent pathways of the interstitial nucleus of Cajal in primate using small tracer injections with Phaseolus lectin and biocytin. It disclosed three projection systems: a commissural, an ascending and a descending pathway.
35. Helmchen C, Rambold H, Büttner U: Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey. Exp Brain Res 1996, 112:63-78. Physiological study of non-premotor saccade-related neurons in the interstitial nucleus of Cajal using three-dimensional eye movement recordings. The properties are compared to those of saccadic premotor burst neurons in the riMLF.
36. Helmchen C, Glasauer S, Bartl K, Büttner U: Contralesionally beating torsional nystagmus in a unilateral rostral midbrain lesion. Neurology 1996, 47:482-486. A small unilateral lesion, thought to affect the riMLF, causes a torsional nystagmus to the contralateral side of the lesion, which is the opposite direction found after a unilateral lesion of the interstitial nucleus of Cajal. A slowing of ipsilateral torsional fast phases was also seen (see [36••]).
37. Riordan-Eva P, Faldon M, Büttner-Ennever JA, Gass A, Bronstein AM, Gresty MA: Abnormalities of torsional fast phase eye movements in unilateral rostral midbrain disease. Neurology 1996, 47:201-207. Small unilateral lesions thought to affect riMLF efferents caused only a slowing of ipsidirectional torsional fast phase eye movements. Compare with [35••].
38. Godaux E, Cheron G: The hypothesis of the uniqueness of the oculomotor neural integrator: direct experimental evidence in the cat. J Physiol Lond 1996, 492:517-527. A recording study in 1he prepositus nucleus of the cat that favours the hypothesis of a unique horizontal oculomotor integrator.
39. Hardy O, Corvisier J: Firing properties of preposito-collicular neurones related to horizontal eye movements in the alert cat. Exp Brain Res 1996, 110:413-424. A recording study demonstrating that preposito-collicular neurons code eye position and eye velocity just like eye muscle motoneurons, suggesting a role in feedback control of an ongoing saccade.
40. Corvisier J, Hardy O: Topographical characteristics of prepositocollicular projections in the cat as revealed by Phaseolus vulgaris-leucoagglutinin technique. A possible organisation underlying temporal-to-spatial transformations. Exp Brain Res 1997, 114:461-471. An anatomical tracing study, which shows that the preposito-collicular (see [38•]) projection is organized in two axonal trajectories; in addition, the projection is weighted along the rostrocaudal axis of the contralateral superior colliculus.
41. Kaneko CRS: Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkey. I. Saccades and fixation. J Neurophysiol 1997, 78:1763-1788. A chemical lesion study of the prepositus nucleus (ppH) with careful histological controls of the damage, demonstrating only minor deficits in gaze holding, no changes of saccades, but impairment of the fixation ability. This paper favours the existence of multiple neuronal integrators rather than of a single multipurpose element (see [37•]), and it contradicts models that rely on feedback control from the ppH (see [38•,39••]).
42. Büttner-Ennever JA, Horn AKE: Pathways from cell groups of the paramedian tracts to the floccular region. Ann NY Acad Sci 1996, 781:532-540. This study demonstrated for the first time the route taken by the paramedian tract (PMT) neurons efferents in the external arcuate fibres to the flocculus and ventral paraflocculus. The PMT cell groups receive inputs similar to the extraocular motoneurons, and could provide the cerebellum with a motor error feedback signal.
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44. 3H]proline, and a critical account of terminology of the area.
45. Ilg UJ, Hoffmann KP: Responses of neurons of the nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic tract in the awake monkey. Eur J Neurosci 1996, 8:92-105. Single-cell recording analyzing the role of NOT/DTN in optokinetic and smooth pursuit eye movements. Unfortunately, no differentiation between NOT and DTN was made.
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47. Büttner-Ennever JA, Cohen B, Horn AKE, Reisine H: Pretectal projections to the oculomotor complex of the monkey and their role in eye movements. J Comp Neurol 1996, 366:348-359. Pretectal projections to a specific set of oculomotor motoneurons (c-group) are verified with transsynaptic retrograde tracer, and suggest a role of the pretectum in the near-response. This is the first attempt to correlate the function of two closely associated components of the pretectum: the NOT and the pretectal olivary nucleus.
48. Miles FA: The sensing of rotational and translational optic flow by the primate optokinetic system. In Visual Motion and Its Role in the Stabilization of Gaze. Edited by Miles FA, Wallman J. Amsterdam: Elsevier; 1993:393-403.
49. Büttner-Ennever JA, Cohen B, Horn AKE, Reisine H: Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements. J Comp Neurol 1996, 373:90-107. A functional analysis of the efferent pathways from NOT, demonstrating that it projects to structures involved in the control of six different types of eye movements. It is suggested that, under the control of the cerebral cortex, NOT could function as a coordinator of the oculomotor circuits to generate the appropriate motor response. The paper emphasizes the importance of considering NOT and DTN as functionally separate structures.
50. Vargas CD, Volchan E, Nasi JP, Bernardes RF, Rochamiranda CE: The nucleus of the optic tract (NOT) and the dorsal terminal nucleus (DTN) of opossums (Didelphis marsupialis aurita). Brain Behav Evol 1996, 48:1-15. A comparison of pretectal cell groups with commissural or inferior olive projections in the opossum. NOT and DTN differ, but are considered as a complex.
51. Reimann S, Schmidt M: Histochemical characterisation of the pretecto-geniculate projection in kitten and adult cat. Dev Brain Res 1996, 91:143-148. This study shows that 50% of the pretecto-geniculate projection neurons are GABAergic, but no projection neurons are calbindin- or parvalbuminimmunoreactive.
52. Schmidt M: Neurons in the cat pretectum that project to the dorsal lateral geniculate nucleus are activated during saccades. J Neurophysiol 1996, 76:2907-2918. Description of a new group of cells in NOT and posterior pretectal nucleus that fire with saccades in the light and darkness (in contrast, the jerk neurons fire only with saccades in light). Unfortunately no differentiation between NOT and DTN was made.
53. Mustari MJ, Fuchs AF, Pong M: Response properties of pretectal omnidirectional pause neurons in the behaving primate. J Neurophysiol 1997, 77:116-125. Description of the physiological properties of a new cell group type in the pretectum that pauses after all saccades.
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55. Ma TP: Saccade-related omnivectoral pause neurons in the primate zona incerta. Neuroreport 1997, 7:2713-2716. This is the first detailed description of another saccade-related group of pause-neurons in the zona incerta of monkey. These cells show a similar firing pattern during saccades as the omnipause neurons in the nucleus raphe interpositus, but they have direct probably GABAergic projections to the superior colliculus (shown in [53••]).
56. Dias EC, Kiesau M, Segraves MA: Acute activation and inactivation of macaque frontal eye field with GABA-related drugs. J Neurophysiol 1995, 74:2744-2748.
57. Stanton GB, Bruce CJ, Goldberg ME: Topography of projections to posterior cortical areas from the macaque frontal eye fields. J Comp Neurol 1995, 353:291-305.
58. Tian JR, Lynch JC: Corticocortical input to the smooth pursuit and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. J Neurophysiol 1996, 76:2754-2771. The authors demonstrate that the smooth pursuit-frontal eye field (FEF) area and saccadic-FEF area have separate afferent sites within the other cortical eye fields. The results imply the parallel flow of smooth pursuit and saccadic information in the cortex rather than a convergence of information. The cebus and macaque monkey have similar cortical eye fields.
59. Leichnetz GR, Gonzalo-Ruiz A: Prearcuate cortex in the Cebus monkey has cortical and subcortical connections like the macaque frontal eye field and projects to fastigial-recipient oculomotor-related brainstem nuclei. Brain Res Bull 1996, 41:1-29. A comprehensive documentation of cortical and subcortical connections of the prearcuate cortex (the putative homologue of the frontal eye field) using horseradish peroxidase tracing.
60. Petit L, Clark VP, Ingeholm J, Haxby JV: Dissociation of saccade-related and pursuit-related activation in human frontal eye fields as revealed by fMRI. J Neurophysiol 1997, 77:3386-3390. The study confirms the location of frontal eye fields (FEFs) in humans and provides evidence for subdivisions into a pursuit and saccade area.
61. Olson CR, Musil SY, Goldberg ME: Single neurons in posterior cingulate cortex of behaving macaque: eye movement signals. J Neurophysiol 1996, 76:3285-3300. Establishes saccade-related properties of a cortical area associated with spatial analysis of visual images.
62. Colby CL, Duhamel JR, Goldberg ME: Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 1997, 76:2841-2852. Provides a clever set of paradigms to tease out the effects of attention and anticipation on parietal eye field cell responses.
63. Carter N, Zee DS: The anatomical localization of saccades using functional imaging studies and transcranial magnetic stimulation. Curr Opin Neurol 1997, 10:10-17.
64. Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL, Rosenberg DR, Carl JR: Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 1996, 75:454-468. Regions of the cerebral cortex in humans involved in different types of saccadic eye movements are localized with respect to the hand-related motor cortex (used here as a landmark). The results appear in agreement with those found in monkey cortex, but the data are extremely difficult to assess anatomically.
65. Petit L, Orssaud C, Tzourio N, Crivello F, Berthoz A, Mazoyer B: Functional anatomy of a prelearned sequence of horizontal saccades in humans. J Neurosci 1996, 16:3714-3726. Exciting results indicating cortical eye fields, basal ganglia and vermis in internally generated saccade-tasks, but difficult to assess anatomically.
66. Barton JJS, Simpson T, Kirikopoulos E, Stewart C, Crawley A, Guthrie B, Wood M, Mikulis D: Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception. Ann Neurol 1996, 40:387-398. A clear discussion on the comparison of human cortical oculomotor function with existing results in monkey. The findings show that an area in the lateral occipitotemporal cortex is related to target motion during pursuit eye movements, and could represent the human homologue of MT. However, additional eye-movement-related inputs to this area suggest that MST may also lie in the same region.