Abstract
Head-fixed gaze shifts were evoked by electrical stimulation of the deeper layers of the cat superior colliculus (SC). After a short latency, saccades were triggered with kinematics similar to those of visually guided saccades. When electrical stimulation was maintained for more than 150–200 ms, postsaccadic smooth eye movements (SEMs) were observed. These movements were characterized by a period of approximately constant velocity following the evoked saccade. Depending on electrode position, a single saccade followed by a slow displacement or a “staircase” of saccades interspersed by SEMs were evoked. Mean velocity decreased with increasing deviation of the eye in the orbit in the direction of the movement. In the situation where a single evoked saccade was followed by a smooth movement, the duration of the latter depended on the duration of the stimulation train. In the situation where evoked saccades converged towards a restricted region of the visual field (“goal”-directed or craniocentric saccades), the SEMs were directed towards the centre of this region and their mean velocity decreased as the eye approached the goal. The direction of induced SEMs depended on the site of stimulation, as is the case for saccadic eye movements, and was not modified by stimulation parameters (“place” code). On the other hand, mean velocity of the movements depended on the site of stimulation and on the frequency and intensity of the current (“rate” code), as reported for saccades in the cat. The kinematics of these postsaccadic SEMs are similar to the kinematics of slow, postsaccadic correction observed during visually triggered gaze shifts of the alert cat. These results support the hypothesis that the SC is not exclusively implicated in the control of fast refixation of gaze but also in controlling postsaccadic conjugate slow eye movements in the cat.
Similar content being viewed by others
References
Adamük E (1870) Ueber der Innervation der Augenbewegungen. Centralbl Med Wiss 5
Barreto JM, Decostre MF, Missal M (1993) Non-causal filtering of biological signals (abstract). Annals of 45th annual reunion of Brasilian Society for Sciences I: 208
Berman AL (1968) The brain stem of the cat: a cytoarchitectonic atlas with stereotaxic coordinates. University of Wisconsin Press, Madison, Wis
Crommelinck M, Roucoux A (1976) Characteristics of cat's eye saccades in different state of alertness. Brain Res 103: 574–578
Crommelinck M, Guitton D, Roucoux A (1977) Retinotopic versus spatial coding of saccades: clues obtained by stimulating deep layers of cat's superior colliculus. In: Baker R, Berthoz A (eds) Control of gaze by brainstem neurons. Elsevier/North-Holland, Amsterdam, pp 425–435
Evinger C, Fuchs AF (1978) Saccadic, smooth pursuit, and optokinetic eye movements of the trained cat. J Physiol (Lond) 285: 209–229
Gottlieb JP, Bruce CJ, MacAvoy MG (1993) Smooth eye movements elicited by microstimulation in the primate frontal eye field. J Neurophysiol 69: 786–799
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, Grantyn R (1976) Synaptic actions of tectofugal pathways on abducens motoneurons in the cat. Brain Res 105: 269–285
Grantyn A, Grantyn R (1982) Axonal patterns and site of termination of cat's superior colliculus neurons projecting in the tectobulbospinal tract. Exp Brain Res 46: 243–256
Grantyn A, Hardy O, Olivier E, Gourdon A (1992) Relationship between task related discharge patterns and axonal morphology of brainstem projection neurons involved in orienting eye and head movements. In: Shimazu H, Shinoda Y (eds) Vestibular and brainstem control of eye, head and body movements. Japan Science Society Press/Karger, Tokyo/Basel, pp 255–273
Guitton D, Mandl G (1977) The frontal eye field in cat. In: Baker R, Berthoz A (eds) Control of gaze by brainstem neurons. Elsevier/North-Holland, Amsterdam, pp 463–467
Guitton D, Munoz DP (1991) Control of orienting gaze shifts by the tecto-reticulo-spinal system in the head-free cat. I. Identification, localization, and effects of behavior on sensory responses. J Neurophysiol 66: 1605–1623
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
Guitton D, Douglas RM, Volle M (1984) Eye-head coordination in cats. J Neurophysiol 52: 1030–1050
Harris LR (1980) The superior colliculus and movements of the head and eyes in cats. J Physiol (Lond) 300: 367–391
Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulata). J Comp Neurol 173: 583–612
Hartwich-Young R, Weber JT (1986) The projections of frontal cortical oculomotor areas to the superior colliculus in the domestic cat. J Comp Neurol 253: 342–357
Huerta MF, Krubitzer LA, Kaas JH (1986) Frontal eye fields as determined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. I. Subcortical connections. J Comp Neurol 253: 415–439
Jeannerod M (1988) The neural and behavioral organization of goal-directed movements. (Oxford psychology series, 15) Clarendon, Oxford
Lefèvre P, Missal M, Galiana HL (1994) Modelling slow correcting movements. J Vestib Res 4: 371–381
McIlwain JT (1986) Effect of eye position on saccades evoked electrically from the superior colliculus of alert cats. J Neurophysiol 55: 97–112
McIlwain JT (1990) Topography of eye-position sensitivity of saccades evoked electrically from the cat's superior colliculus. Visual Neurosci 4: 289–298
Missal M, Lefèvre P, Crommelinck M (1994) Evidence for high velocity smooth pursuit eye movements in the cat. Soc Neurosci Abstr 20: 359.11
Missal M, Crommelinck M, Roucoux A, Decostre MF (1993) Slow correcting eye movements of head-fixed, trained cats toward stationary targets. Exp Brain Res 96: 65–76
Munoz DP, Pélisson D, Guitton D (1991) Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251: 1358–1360
Olivier E, Gratyn A, Chat M, Berthoz A (1993) The control of slow orienting movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections. Exp Brain Res 93: 435–449
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
Peck CK (1987) Saccade-related burst neurons in cat superior colliculus. Brain Res 408: 329–333
Ron S, Robinson DA (1973) Eye movements evoked by cerebellar stimulation in the alert monkey. J Neurophysiol 36: 1004–1022
Ron S, Berthoz A, Gur S (1993) Saccade vestibulo-ocular reflex cooperation and eye-head uncoupling during orientation to flashed target. J Physiol (Lond) 464: 595–611
Roucoux A, Guitton D, Crommelinck M (1980) Stimulation of the superior colliculus in the alert cat. II. Eye and head moveents evoked when the head is unrestrained. Exp Brain Res 39: 75–85
Schiller PH, Koerner F (1971) Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. J Neurophysiol 34: 920–936
Stein BE, Goldberg SJ, Clamann HP (1976) The control of eye movements by the superior colliculus in the alert cat. Brain Res 118: 469–474
Straschill M, Rieger P (1973) Eye movement evoked by focal stimulation of the cat's superior colliculus. Brain Res 59: 211–227
Yamada T, Suzuki DA, Betelak KF, Yee RD (1991) Initial eye position dependence of eye movements evoked by microstimulation in the monkey nucleus reticularis tegmenti pontis. Soc Neurosci Abstr 17: 459
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Missal, M., Lefèvre, P., Delinte, A. et al. Smooth eye movements evoked by electrical stimulation of the cat's superior colliculus. Exp Brain Res 107, 382–390 (1996). https://doi.org/10.1007/BF00230420
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00230420