THE PRETRIGEMINAL CAT AS AN INSTRUMENT FOR INVESTIGATION OF THE OCULAR FIXATION REFLEX

Transcription

1 ACTA NEUROBIOL. EXP. 1980, 40: Lecture delivered at the Warsaw Colloquium on Instrumental Conditioning and Brain Research May 1979 THE PRETRIGEMINAL CAT AS AN INSTRUMENT FOR INVESTIGATION OF THE OCULAR FIXATION REFLEX Department of Neurophysiology, Nencki Institute of Experimental Biology Warsaw, Poland Abstract. The fixation reflex is an important representative of orienting (targeting) reflexes. In the cat with the brainstem transected at the pretrigeminal level the fixation reflex is easy to investigate for the following reasons: (a) all sensory inputs to the isolated cerebrum of the pretrigeminal cat are eliminated, except for visual afferents, (b) the isolated cerebrum is continuously awake, (c) the vertical fixation reflex only is present. The behavioral and neural characteristics of the fixation reflex in the pretrigeminal cat are reviewed. An important class of behavior is represented by reflexes which adjust a given analyzer to the better perception of a stimulus (13, p. 17). These reflexes, denoted as orienting or targeting (13), operate almost continuously. Good examples are long-term watching of the TV or a lecturer. In spite of the importance of targeting reflexes, their properties and central mechanisms are poorly known. The obvious reason is that these reflexes are present only in the awake animal, in which it is difficult to record them precisely. A conspicuous representative of targeting reflexes is ocular fixation reflex. This reflex brings the image of the object on the area centralis and maintains the image in this position for a while. The fixation reflex consists of three phases: (a) a saccadic movement towards the object, (b) maintenance of the fixation, (c) a return saccadic movement. When an object moves slowly and at constant speed in the

2 visual field, the maintenance phase consists of a following (pursuit) movement, which matches that of the stimulus. Such a reflex is called the following reflex (6). The cat with a brainstem transection at the pretrigeminal level (1, 22) is a valuable instrument for investigating the fixation reflex. The isolated cerebrum of the pretrigeminal cat is awake and controls the vertical fixation reflex, which does not seem to differ significantly from that in the i'ntact cat (25). The three main advantages of the pretrigeminal cat over an intact animal as an instrument for investigating the fixation reflex are as follows: 1. Visual input only to the cerebrum is preserved. Olfactory input is eliminated by tracheotomy which usually precedes the pretrigeminal transection. Thus the effects of a visual stimulus are not obscured by those due to other stimuli. Moreover, the optokinetic reflex (optokinetic nystagmus) is absent (12). The lack of pain is particularly important. The cat can be restrained in the stereotaxic apparatus without local anesthesia, and the position of the eye can be monitored using simple techniques. I,n our experiments we use a tensometric method (8). The lower margin of the eye is attached with a thread to a hair spring connected to a tensometric transducer. The vertical position of the eye is displayed continuously on an oscillosco~pe. The sensitivity of the method is 20'. 2. During an experiment the level of wakefulness of the isolated cerebrum usually remains stable. In the acute stage the cerebrum is either alert or drowsy and shifts 'between these two stages occur infrequently, on average, llh (20). 3. Horizontal eye movements are absent in the pretrigeminal cat (the center controlling them is caudal to the transection). The lack of the horizontal fixation reflex is convenient for two reasons: (a) only the vertical position of the eye need to be monitored, (b) a stimulus presented at the lateral or medial part of the visual field is not brought on to the area centralis (see below). Three disadvantages of the pretrigeminal cat in comparison with an intact cat should be also mentioned: 1. Nursi.ng care of the chronic cats is tedious and the experiments are performed preferably on acute preparations. 2. Some acute preparations (about 30 /o) are semicomatose or comatose and then the fixation reflex is abortive or absent, respectively (22). In such cases, however, the administration of a small dose of amphetamine (0.5-1 mg i.v.) is usually helpful. The amphetamine also greatly increases the resistance to habituation of the fixation reflex (5).

3 3. Establishment of a conditioned fixation reflex is less easy than in the intact animal, in which natural reinforcement is available (juice or milk is usually given directly into the mouth). However, by using electrical stimulation of the lateral hypothalamus as a reinforcement, conditioned eye movements can be established in the pretrigeminal cat (10, 11, 18, 26). In our Laboratory the pretrigeminal cat has been used for several years in investigation of the vertical fixation reflex. The principal findings are as follows: 1. The following reflex can 'be evoked by a stimulus presented in the lateral or medial hemifield (Fig. 1). Duri'ng the following phase Fig. 1. Following reflexes to the stick (1 X 4") moving upwards at different distances from the vertical meridian during a representative experimental session. Four reflexes at each distance averaged are indicated by the heavy line and the movement of the stick with a fine line. The small oscillations represent principally noise from the recording system. The small numbers indicate the order of recording. Ordinate: inclination of the eye. Note that the resting position of the eye was continuously low, occasionally even lower than the stimulus onset position. From Michalski et al. (15). the image of the stimulus is held on the horizontal meridian, i.e. on the visual streak of highest ganglion cell density (9). Thus, the following reflex can be controlled by the peripheral retina. 2. The fixation reflex becomes abortive and habituates easily following ablation of the visual cortex, and it is absent followi,ng removal of the superior colliculi (3). On the other hand, ablation of the frontal eye fields (4) enhances the duration of the fixation reflex (5, 21). In particular, its resistance to habituation is increased. In the isolated

4 midbrain with visual input preserved (the brainstem is transected at the pretrigeminal and "preoptic" levels) the fixation reflex is absent (24). Although in the isolated midbrain the EEG activity is depressed (23, 24), the responses of collicular units to moving visual stimuli are almost normal (2). 3. In cats visually deprived.from 'birth-the fixation reflex is only slightly impaired (14). Thus the development of the fixation reflex is predominantly on a genetic basis. 4. During the pursuit (following) stage of the following reflex about 20 /0 of the units in the rapresentation of the.area centralis in cortical areas 17 and 18 change their activity, presumably as the effect of a "corollary discharge" from the frontal eye fields (16). 11n this study the stimulus moved vertically with horizontal eccentricity of 40, i.e. beyond the receptive fields of the units tested. 5. The intensity of the fixation reflex (as measured by the duration of fixation) is positively correlated with several other ocular and cerebral responses to the visual stimulus: (a) the intensity of pupillary dilatation and cortical EEG desynchronization (25), (b) the level of increase in regularity and frequency of the hippocampal theta activity (17), (c) the level of increase in cerebral blood flow in the occipital and frontal cortex (19), (d) presumably the duration of visual accommodation (7). 1. BATINI, C., MORUZZI, G., PALESTINI, M., ROSSI, G. F. and ZANCHETTI, A Effects,of complete pontine transections on the sleep-wakefulness rhythm: the midpontine pretrigeminal preparation. Arch. Ital. Biol. 97: DEC, K., TARNECKI, R. and ZERNICKI, B Single unit reslponses to moving spots in the superior colliculus of the cat's isolated midbrain. Acta Neurobiol. Exp. 38: DRE'HER, B., MARCHIAFAVA, P. L. and ZERNICKI, B Studies on the visual fixation reflex. 11. The neural mechanism of the fixation reflex in normal and pretrigeminal cats. Acta Bimol. Exp. 25: DREHER, B., SANTIBAREZ-H., G. and ZERNICKI, B Oculomotor cortex localization in the unanesthetized cat. Acta Neurobiol. Exp. 30: DREHER, B. and ZERNICKI, B Studies on the visual fixation reflex The effects of frontal lesions in the cat. Acta Biol. Exp. 29: DREHER, S. and ZERNICKI, B Visual fixation reflex: behavioral properties and neural mechanimsm. Acta Bi,ol. Exp. 29: FLUL, R. and MARCHIAVAVA, P. L Accommodation of the eye as related to behavior in the cat. Amch. Ital. Biol. 102: FOLGA, J., MICHALSKI, A,, TURLEJSKI, K. and ZERNICKI, B Eyemovement recording with a tensometric method in the pretrigeminal cat. Acta Neurobiol. Exp. 33:

5 9. HUGHES, A A quantitative analysis of the cat retinal ganglion cell topography. J. Comp. Neurol. 163: IKEGAMI, S., NISHIOKA, S. and KAWAMURA, H Operant conditioning of vertical eye movements without visual feedback in the midpontine pretrigeminal cat. Brain Res. 169: IKEGAMI, S., NISHIOKA, S. and KAWAMURA, H. 19'77. Operant discriminative conditioning of vertical eye movements in the midpontine pretrigeminal cat. Brain Res. 124: KING, F. A. and MARCHIAFAVA, P. L Ocular movements in the midpontine pretrigeminal preparation. Arch. Ital. Biol. 101: KONORSKI, J Integrative activity of the brain. An interdisciplinary approach. Univ. Chicago Press, Chicago, 531 p. 14. KOSSUT, M., MICHALSKI, A. and ZERNICKI, B The ocular following reflex in cats deprived of pattern vision from birth. Brain Res. 141: MICHALSKI, A., KOSSUT, M. and ZERNICKI, B The ocular following reflex elicited from the retinal periphery in the cat. Vision Res. 17: MICHATSKI, A. and MOROZ, B The effects of pursuit eye movements on single unit activity i~n cat visual cortex. Acta Neurobiol. Exp. 37: RADIL-WEISS, T., ZERNICKI, B. and MICHALSKI, A Hippocampal theta activity in the acute pretrigeminal cat. Acta Neurobiol. Exp. 36: SHLAER, R. and MYERS, M. L Operant conditioning of the pretrigeminal cat. Brain Res. 38: SKOLASINSKA, K., KROLICKI, L. and ZERNICKI, B Regional cerebral blood flow and visual attedtion in the awake isolated cerebrum of the pretrigeminal cat. Acta Neurobiol. Exp. 39: SL~SARSKA, M. and ZERNICKI, B Wakefulness and sleep in the isolated cerebrum of the pretrigemi'nal cat. Arch. Ital. Biol. 109: ZERNICKI, B Orienting response hypernormality in frontal cats. Acta Neurobiol. Exp. 32: ZERNICKI, B Isolalted cerebrum of the pretrigeminal cat. Arch. Ital. Biol. 112: ZERNICKI, B., DEC, K., SARNA, M., JASTREBOFF, P. and VERDEREV- SKAYA, N Single-unit activity in the cat's isolated midbrain. Acta Neurobiol. Exp. 39: ZERNICKI, B., DOTY, R. W. and SANTIBAREZ-H., G Isolated midbrain in cats. Electroenceph. Clin. Neurophysiol. 28: ZERNICKI, B. amnd DREHER, B Studies on the visual fixation. I. General lproperti,es of the orientation fixation reflex in pretrigeminal and intact cats. Acta Biol. Exp. 25: ZERNICKI, B., MICHALSKI, A., RADIL-WEISS, T. and KqCZKOWSKA, E Instru~mental ocular conditioning in acute pretrigeminal cat. Acta Neurobiol. Exp. 38: Boguslaw ZERNICKI, Nencki Institute of Experimental Biology, Pasteura 3, Warsaw, Poland Acta Neurobiologiae Exp. 1180