The superior colliculus and eye movement control

Current Opinion in Neurobiology

Volumn 6, Issue 6, 1996, Pages 811-816

  Moschovakis, Adonis K ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROSTIMULATION; EYE MOVEMENT CONTROL; NONHUMAN; PRIMATE; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SHORT SURVEY; SUPERIOR COLLICULUS;

EID: 0030475105     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(96)80032-8     Document Type: Article

References (55)

1. Moschovakis AK, Scudder CA, Highstein SM: The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol 1996, 50:133-254. A comprehensive review of the response properties, appearance and connections of 30 distinct classes of neurons that have been implicated so far in the control of rapid eye movements. The authors evaluate the performance of several models of the saccadic system and include a point by point comparison of the relative merits of the 'foveation1, 'spatial' and 'vector subtraction' hypotheses of tectal function.
2. Moschovakis AK, Highstein SM: The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 1994, 17:465-488.
3. Sparks DL: Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset Brain Res 1978, 156:1-16.
4. Groh JM, Sparks DL: Saccades to somatosensory targets. II. Motor convergence in primate superior colliculus. J Neurophysiol 1996, 75:428-438.
5. Sparks DL, Mays LE: Movement fields of saccade-related burst neurons in the monkey superior colliculus. Brain Res 1980, 190:39-50.
6. Sparks DL, Holland R, Guthrie BL: Size and distribution of movement fields in the monkey superior colliculus. Brain Res 1976, 113:21-34.
7. Munoz DP, Wurtz RH: Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol 1995, 73:2313-2333. An extracellular recording study in trained rhesus monkeys that carefully reevaluates the discharge pattern of tectal pre-saccadic neurons. The majority of encountered pre-saccadic cells (67%) emitted a burst of discharge just before saccade onset. The remaining cells (33%) displayed a build-up of activity that followed the presentation of visual stimuli and ended together with saccades to them. The build-up of discharge is not necessary for the occurrence of saccades, as it can develop in their absence. Unlike burst cells, most build-up neurons discharged for all saccades bigger than a certain size. Build-up neurons also differ from burst cells in that they are located more ventrally in the SC.
8. Mohler CW, Wurtz RH: Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J Neurophysiol 1976, 39:722-744.
9. Mays LE, Sparks DL: Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 1980, 43:207-232.
10. Munoz DP, Wurtz RH: Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 1993, 70:559-575.
11. Moschovakis AK, Karabelas AB, Highstein SM: Structurefunction relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J Neurophysiol 1988, 60:263-302.
12. Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM: Anatomy and physiology of saccadic long-lead burstneurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon. J Neurophysiol 1996, 76:332-352. This intra-axonal recording and horseradish peroxidase injection study in alert behaving monkeys is the first to provide a description of the targets of crossed descending TLLB fibers. Their relatively small diameter and their frequent responses to stimulation of the contralateral as well as of the ipsilateral SC strongly support the notion that they originate from cells that belong to the T class of tectal efferent neurons [13,14,41]. This study is also the first to describe the morphological and physiological features of long-lead burst neurons that are located in the mesencephalic reticular formation and that project to the pons.
13. Moschovakis AK, Karabelas AB: Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat J Comp A/euro/1985, 239:276-308.
14. Karabelas AB, Moschovakis AK: Nigral inhibitory termination on efferent neurons of the superior colliculus. An intracellular horseradish peroxidase study in the cat J Comp Neurol 1985, 239:309-329.
15. Büttner U, Büttner-Ennever JA, Henn V: Vertical eye movement related activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res 1977, 130:239-252.
16. King WM, Fuchs AF: Neuronal activity in the mesencephalon related to vertical eye movements. In Control of Gaze by Brain Stem Neurons. Edited by Baker R, Berthoz A. Amsterdam: Elsevier; 1977:319-326.
17. Moschovakis AK, Scudder CA, Highstein SM: A morphological basis for Hering's law: projections to extraocular motoneurons. Science 1990, 248:1118-1119.
18. Moschovakis AK, Scudder CA, Highstein SM, Warren JD: Structure of the primate burst generator. II. Medium-lead burst neurons with downward on-directions. J Neurophysiol 1991, 65:218-229.
19. Moschovakis AK, Scudder CA, Highstein SM: Structure of the primate burst generator. I. Medium-lead burst neurons with upward on-directions. J Neurophysiol 1991, 65:203-217.
20. Luschei ES, Fuchs AF: Activity of brain stem neurons during eye movements of alert monkeys. J Neurophysiol 1972, 35:445-461.
21. Strassman A, Highstein SM, McCrea RA: Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons. J Comp A/euro/1986, 249:358-380.
22. Strassman A, Highstein SM, McCrea RA: Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 1986, 249:337-357.
23. Scudder CA, Fuchs AF, Langer TP: Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. J Neurophysiol 1988, 59:1430-1454.
24. 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 intra-axonal recording and horseradish peroxidase injection study in alert monkeys is the first to provide a description of the physiological and anatomical features of primate pontine long-lead burst neurons (LLBs). Three cell classes were described: pre-cerebellar neurons displaying a discharge pattern similar to that of directional or vectorial LLBs and sending axonal projections to the cerebellum; reticulospinal neurons displaying a discharge pattern similar to that of directional LLBs and sending axonal projections to the spinal cord; and ponto-pontine cells deploying local terminal fields in the reticular formation of the pons.
25. Strassman A, Evinger C, McCrea RA, Baker RG, Highstein SM: Anatomy and physiology of intracellularly labelled omnipause neurons in the cat and squirrel monkey. Exp Brain Res 1987, 67:436-440.
26. Robinson DA: Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 1972, 12:1795-1808.
27. Straschill M, Rieger P: Eye movements evoked by focal stimulation of the cat's superior colliculus. Brain Res 1973, 59:211-227.
28. Mcllwain JT: Effects of eye position on saccades evoked electrically from the superior colliculus of alert cats. J Neurophysiol 1986, 55:97-112.
29. Mcllwain JT: Topography of eye-position sensitivity of saccades evoked electrically from the cat's superior colliculus. Vis Neurosci 1990, 4:289-298.
30. Hepp K, Van Opstal AJ, Straumann D, Hess BJM, Henn V: Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. J Neurophysiol 1993, 69:965-979.
31. Russo GS, Bruce CJ: Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields. J Neurophysiol 1993, 69:800-818.
32. Van Opstal AJ, Hepp K, Suzuki Y, Henn V: Influence of eye position on activity in monkey superior colliculus. J Neurophysiol 1995, 74:1593-1610. An extracellular recording study of the discharge pattern of primate tectal pre-saccadic neurons. The discharge of about half of the cells was shown to depend on the position of the eyes at saccade onset, albeit modestly. Conceivably, the movement fields of these cells result from the convolution of a Gaussian function of two spatial dimensions and a planar gain field. As expected of cells contributing to compensation of orbital non-linearities, gain fields collinear with the cells' preferred directions were observed. However, this was the case for about half of the cells; in addition, oppositely or orthogonally directed gain fields were often observed.
33. Grantyn AA, Dalezios Y, Kitama T, Moschovakis AK: 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 1996, 41:65-82. This is a quantitative study of rapid (saccades) and slow (drifts) eye movements produced in response to the electrical stimulation of the SC in alert, head-fixed cats. The authors demonstrate that the intensity of the stimulation, the electrode location and the initial position of the eyes influence in a similar manner the amplitude and direction of both saccades and slow drifts. Slow drifts are also characterized by several other facts: first, that they last for the duration of stimulation; second, that their size increases with the frequency of stimulation (which implies that they are due to the engagement of a portion of the oculomotor system that operates in the frequency domain); and finally, that their trajectories are exponential or ramp-like (which implies that they are attributable to collicular projections upon extraocular motoneurons, either directly or via the velocity to position integrators). Because of their similar properties, despite their control by dissimilar circuits, the position sensitivity of evoked saccades and slow drifts could be attributable to the same peripheral mechanism.
34. Missal M, Lefèvre 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. A second study of the slow eye movements that are evoked in response to the electrical stimulation of the SC in alert, behaving, head-fixed cats. It pays particular attention to the effect of stimulation parameters upon movement velocity and confirms the fact that the kinematics of evoked slow eye movements depends on the initial position of the eyes. However, the authors' conclusion that evoked slow eye movements correspond to smooth pursuit ones and that the SC participates in the control of smooth pursuit eye movements is unwarranted.
35. Grantyn A, Grantyn R: Axonal patterns and sites of termination of cat superior colliculus neurons projecting to the tectobulbo-spinal tract Exp Brain Res 1982, 46:243-256.
36. Grantyn A, Berthoz A: Burst activity of identified tectoreticulospinal neurons in the alert cat Exp Brain Res 1985, 57:417-421.
37. Grantyn A, Ong-Meang J, Berthoz A: Reticulospinal 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 1987, 66:355-377.
38. Nichols MJ, Sparks DL: Nonstationary properties of the saccadic system: new constraints on models of saccadic control. J Neurophysiol 1995, 73:431-435. A study of the metrics of saccades evoked in response to the electrical stimulation of the SC after a previous visually guided saccade to test the predictions of two models of the saccadic burst generator. The comparator of the first model (eye position model) subtracts an eye position signal from the desired eye position signal to create the signal that drives burst neurons. The burst generator of the second model (eye displacement model) is driven by the difference between a desired eye displacement command and the output of a leaky integrator (which integrates the output of the burst generator [51]). Consistent with the eye displacement model, but not with the eye position model, the amplitude and direction of evoked saccades are shown to depend systematically on the amplitude and direction of the preceding visually guided saccades. The effect decays exponentially with a time constant equal to about 50 ms (the presumed time constant of the leaky integrator). The size and direction of evoked saccades approach exponentially the values attained by saccades usually evoked from the same site. This implies that the mechanism that resets the integrator may rely more on the latter's inherent leakiness than on an active process. See also [39].
39. Kustov AA, Robinson DL: Modified saccades evoked by stimulation of the macaque superior colliculus account for properties of the resettable integrator. J Neurophysiol 1995, 73:1724-1728. The second study (see [38]) to demonstrate that the amplitude and direction of saccades evoked after electrical stimulation of the SC depends systematically on the amplitude and direction of preceding visually guided saccades. It confirms that the effect decays exponentially with a time constant equal to the presumed time constant of an eye displacement feedback signal. Consistent with the 'vector subtraction' hypothesis, subtraction of the feedback vector from the Tr signal (represented by the location of the electrode in the SC) predicts evoked saccades of correct metrics.
40. Schiller PH, Koerner F: Discharge characteristics of single units in the superior colliculus of the alert rhesus monkey. J Neurophysiol 1971, 34:920-936.
41. Moschovakis AK, Karabelas AB, Highstein SM: Structurefunction relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J Neurophysiol 1988, 60:232-262.
42. Sparks DL, Mays LE: Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. J Neurophysiol 1983, 49:45-63.
43. Moschovakis AK: Neural network simulations of the primate oculomotor system. II. Frames of reference. Brain Res Bull 1996,40:337-345. This study is a disproof by counter-example of the often enunciated assumption that the location of visual targets must be expressed in a head-centered frame of reference for the brain to issue commands to execute accurate foveating saccades. Evidence from the burst generators in the reticular formation of the brain stem and the metric computer in the superior colliculus is evaluated to show that saccades can be programmed and executed in a retinotopic frame of reference provided that the representation of target location is updated after each saccade.
44. Walker MF, Fitzgibbon EJ, Goldberg ME: Neurons in the monkey superior colliculus predict the visual result of impeding saccadic eye movements. J Neurophysiol 1995, 73:1988-2003. The authors demonstrate that a minority (about 30%) of the visuo-movement cells of the deeper tectal layers discharge for a visual stimulus that lies outside the cell's receptive field but is brought in it by a saccade executed soon thereafter. The neuron's response is predictive because it precedes the movement by more than 50 ms, whereas the visual stimulus enters the cell's receptive field after saccade onset. Timing considerations make it difficult to reconcile this finding with the notion that an eye position signal is needed to compute target location and saccade metrics. In contrast, the predictive visual response of deeper tectal layer cells is consistent with the 'vector subtraction' hypothesis [2,11].
45. Dassonville P, Schlag J, Schlag-Rey M: The use of egocentric and exocentric location cues in saccadic programming. Vision Res 1995, 35:2191-2199. One of several recent articles (see e.g. [46]) that cast doubt on the ability of humans to accurately localize visual targets flashed shortly before the onset of a saccade. In the presence of other visual stimuli, localization errors were sometimes small but could not be completely eliminated.
46. r→ signal and an eye displacement signal (carried by long-lead burst neurons). Because long-lead burst neurons discharge shortly before saccades, the illusion would result from the fact that the eye displacement signal is absent at the time of the first flash but present at the time of the second flash (shortly before saccade onset).
47. 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 detailed study of the response properties of long-lead burst neurons (LLBs) in the central mesencephalic reticular formation (cMRF) of the rhesus monkey. Neurons responsive or unresponsive to visual targets, 'clipped' or 'partially clipped' burst offset and high or low background firing rates, were found. The time course of their discharge is shown to reflect eye displacement and/or eye velocity. Timing considerations indicate that the discharge of cMRF LLBs follows rather than leads the onset of saccade-related activity in the SC. The cells described in this study could correspond to either class of cMRF LLBs, namely RTLLBs [11] or LLBs that project to the paramedian pontine reticular formation [12]. Engagement of these cells presumably accounts for the demonstration that the amplitude and direction of saccades evoked in response to the electrical stimulation of the cMRF correlate well with the optimal movement vectors encoded by neighboring cells. It is difficult to determine the extent to which evoked saccades also reflect the engagement of TLLB axons coursing through this area.
48. Droulez J, Berthoz A: A neural network model of sensoritopic maps with predictive short-term memory properties. Proc Natl Acad Sei USA 1991, 88:9653-9657.
49. Waitzman DM, Ma TP, Optican LM, Wurtz RH: Superior colliculus neurons mediate the dynamic characteristics of saccades. J Neurophysiol 1991, 66:1716-1737.
50. Munoz DP, Guitton D, Pelisson D: Control of orienting gaze shifts by the tecto-reticulo-spinal system in the head-free cat III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 1991, 66:1642-1666.
51. Moschovakis AK: Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. Biol Cybern 1994, 70:291-302.
52. Das S, Gandhi NJ, Keller EL: Open-loop simulations of the primate saccadic system using burst cell discharge from the superior colliculus. Biol Cybern 1995, 73:509-518. Evaluates the verisimilitude of saccades produced by a model of the burst generator fed with the discharge of real TLLBs. Despite the fact that it operated without its feedback path, the model produced fairly realistic saccades of various sizes to the centers of the cells' movement fields. Signals used to drive the model's burst generator included the digitized discharge of TLLBs for saccades interrupted by the electrical stimulation of the omnipause area. The model accurately reproduced the mid-flight interruption of saccades observed in such circumstances.
53. Munoz DP, Wurtz RH: Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J Neurophysiol 1995, 73:2334-2348. Provides estimates of the spatial extent of activation of the deeper tectal layers of primates for saccades of different sizes. The average diameter of the spread of excitation among build-up cells is equal to 2 mm of tectal space for a 5' saccade and more than 3 mm for a saccade greater than or equal to 20'. It equals 1.4 ±0.3 mm for TLLBs, and scales little with eccentricity. Also, the authors attempt to modify the hypothesis that a caudo-rostral wave of discharge moves through the deeper tectal layers during saccades [50]. It is claimed that the time course of the discharge of burst and build-up neurons supports the notion that a wave of discharge moves through build-up cells and not TLLBs. It is difficult to reconcile these claims with the fact that the discharge of build-up neurons often lacks a definite onset and peak, thus impeding any attempts to accurately evaluate the time difference between neural events and motor acts. Actually, this study provides data from 30 saccades that demonstrate that all build-up neurons throughout the SC are active when saccades take off and that they are not sequentially activated from back to front. Even if proven, such a wave of discharge need not be causally relevant for saccades, as it does not seem to influence either the spatial distribution or the time course of the discharge of the much more numerous TLLBs that connect the SC with the burst generators.
54. Keller EL: Control of saccadic eye movements by midline brainstem neurons. In Control of Gaze by Brainstem Neurons. Edited by Baker R, Berthoz A. Amsterdam: Elsevier; 1977:327-336.
55. Keller EL, Edelman JA: Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccade burst cells in superior colliculus in monkey. J Neurophysiol 1994, 72:2754-2770.