The response of rabbit ciliary nerve to luminance intensity

206

Bratn Research, 201 (1980) 206 209 :c) Elsewer/North-Holland Biomedical Pre~.~

The response of rabbit ciliary nerve to luminance intensity

TAKAMICHI INOUE Department of Physiology, Ntppon Medical School, 1-1-5, Sendagt, Bunkyo-ku, Tokyo (Japan) (Accepted July 10th, 1980) Key words: cdmry nerve - - type A umt - - pupillo-constnctor umt - - pupdlary hght reflex - - luminance intensity - - rabb~t

Using cerwcal sympathectomlzed and ~mmobd~zedrabbits, the relatmnshlp between the luminance intensity and the magnitude of the response in pupillo-constrictor units of the ciliary nerve was investigated. It was revealed that the intensity - response relationship of the umts closely resembled that of retmal receptors. Therefore, it would seem that retinal information concerning luminance ~s relayed wtthout alteratton to the cdiary nerve m spite of passing through a number of synapses. The so-called 'on-umts', which show excitatory responses to light stimuli, exist in the cihary nerve 4-7,t°. It seems that these units mediate the pupillary light reflex. On the other hand, concerning inputs to pupillo-constrictor umts o f the ciliary nerve, 'luminance units '1 or 'tonic on-center W-cells '15 o f retinal ganghon cells and ' t o m c - o n units' m the pretectum 0,12,~4 and the o c u l o m o t o r nucleus 13 have been indicated. The relationship between the intensity o f the stimulating light and the firing rate o f these units, however, has not been e x a m m e d in detail. This report describes the relattonshlp based on the studies carried out m rabbits. The albino rabbits were lightly anaesthetized by pentobarbital s o d m m (Nembutal) immobilized with D-tubocurarine, and maintained on artificial respiration. In addition, the cervical sympathetic nerves were transected on both sides. The left upper eyelid was incised on the median line, the supraorbital bone was removed, and then the superior rectus, the superior oblique and a part o f the retractor bulbi muscle were severed at their insertions into the sclera m order to expose the cihary nerves. The exposed sclera was covcred with R i n g e r - A g a r solution and the orbit was filled with w a r m paraffin od. Efferent discharges from the proximal stumps o f the ciliary nerves were recorded m o n o polary by means o f a platinum wire electrode (200/~m in diameter) in the paraffin pool. Signals were amplified and displayed by the conventional methods. The details of the experimental procedure are described elsewhere 6. As a light stimulus, a diffuse light source was provided by a xenon lamp, and the light intensity was controlled with neutral density filters. The pupil of the eye under study was dilated w~th atropine in order to study the fundamental intensity-response relationship o f pupiUo-constrictor units (open-loop condition). In the previous work 5,6 two kinds o f units were distinguished according to their response patterns to diffuse light: 1, the type A unit which responded with excitation

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in each record indicates the time during which the eye is illuminated (exposure = 1.4 see). The intensity (log units) of the test light is indicated on the left of each recording. The brightest luminance (6.0 log units) dehvered about 6300 ft cd on the surface of the cornea. (increase in firing rate) to light stimuli applied to the ipsilateral eye with respect to the site of recording; and 2, the type B unit which responded with inhibition (decrease in firing rate) ipsilaterally and/or contralaterally. The present report deals with the response of the type A unit to the ipsilateral stimulation of various intensities. Fig. 1 shows an example of the type A response to the ipsilateral illumination at various intensities. In order to maintain a steady level of the spontaneous discharge of the type A unit before stimulation, the mterval between test lights was lengthened from 30 sec for dim test lights to some minutes for the bright ones. As shown in the figure, units of this type responded by a high rate of discharge initially, then followed by a sustained discharge which continued as long as the stimulus was present. As the intensity of the test light was increased, the magnitude of both the initial and the steady state response increased in a graded manner. They exhibited, in general, a low frequency spontaneous discharge as shown in Fig. 1, and the spontaneous firing fluctuated depending upon the level of anaesthesia or sleep. Further, the maximum firing rate of the response and the spontaneous firing varied in different units. However, this seems to be a physiological phenomenon rather than to be due to the damage created by operation or recording. Fig. 2 gives the relation between luminance intensities and sustained responses of type A umts in 0.5 log unit steps from 0.063 to 0.063 x 105 ft cd. The initial phase of the response will be described later. The data used in this figure were obtained from 5 different units. First, the difference between the sustained response and the spontaneous firing just before the stimulus was calculated as the magnitude of each response. The

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period of 1 see beginning at 400 msec after the onset of the stimulation was used in the calculation as the sustained phase, then the calculated values from each umt were normalized and plotted against the logarithm o f light intensity. The minimum test intensity that elicited the type A response distinguishable from spontaneous fluctuation was about 2.0-2.5 log units which corresponded to 0.63-2.0 ft cd. The intensity-response relationship of the sustained level of the type A unit was S-shaped, and in the middle portion the relation was linear within the range o f I log unit and the total response range was nearly 4 log units. In Fig. 2 the interrupted line plots the equation: F Fmax

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where F is the firing rate of the sustained level of the hght-evoked response at intensity I, Fmnx is the maximal response of the sustained phase, and tr is the intensity necessary to give a response of 1/2 Fmax. This equation has been shown first to describe the intensity-response curve of S-potentials s and then the receptors2,a. 11 in the retina. On the other hand, in the present experiments the intensity-response relationship during the initial phase (i.e. the period of 400 msec starting from the onset of the light-evoked response) also showed a similar S-shape curve which shifted to the left, to some extent, along the luminance axis from the curve of the sustained response indicated above. Thus, the intensity-response curve of the type A unit m the rabbit's ciliary nerve also closely fits this equation. Although type A units are classified into AI, A t [ and AI[1 on the basis of the response to the contralateral stimulation (see ref. 6), the properties of the response to the ipsilateral stimulation described above were identical in the 3 sub-types. Therefore, ~t seems that retinal information concerning luminance is relayed to the ciliary nerve without undergoing much transformation in spite of passing through polysynaptic pathways.

209 In all, 25 units were examined under similar conditions and in all cases the responses were similar to those described above. Further, similar results were obtained (also in type A units) from pigmented rabbits. I wish to thank Prof. Y. Fujita and Dr. J. Kaizawa for offering many helpful suggestions throughout this study. I also wish to thank Miss Hamada for preparing the photographic prints.

1 Barlow, H. B. and Levick, W. R., Changes in the maintained discharge with adaptation level in the cat retina, J. Physiol. (Lond.), 202 (1969) 699-718. 2 Baylor, D. A. and Fuortes, M. G. F., Electrical responses of single cones in the retina of the turtle, J. Physiol. (Lond.), 207 (1970) 77-92. 3 Boynton, R. M. and Whltten, D. N., Visual adaption in monkey cones: recordings of late receptor potentials, Science, 170 (1970) 1423-1425. 4 Hultborn, H., Mori, K. and Tsukahara, N., The neuronal pathway subserving the pupillary light reflex, Brain Research, 159 (1978) 255-267. 5 Inoue, T., Efferent impulses in the long and short cdlary nerve of rabbit, J. physiol. Soc. (Jap), 38 (1976) 132. 6 Inoue, T., Efferent &scharge patterns in the ciliary nerve of rabbits and the pupillary light reflex, Brain Research, 186 (1980) 43-53. 7 Melnitchenko, L. V. and Skok, V. I., Natural electrical activity in mammalian parasympathetic ganglion neurones, Brain Research, 23 (1970) 277-279. 8 Naka, K. and Rushton, W. A. H., S-potentials from luminocity units in the retina offish (Cyprinidae), J. Physiol. (Lond.), 185 (1966) 587-599. 9 Nishida, I., Okada, H. and Nakano, O., Electrical activity of the pretectal region of the cat to visual stimulus, Yonago Acta reed, 4 (1959) 7-19. l0 Nishida, I. and Okada, H., The activity of the pupilloconstrictory centers, Jap. J. Physiol., l0 (1960) 64-72. I l Normann, R. A. and Werbhn, F. S., Control of retinal sensitivity: I. Light and darkadaptation of vertebrate rods and cones. J. gen. Physiol., 63 (1974) 37-61. 12 Sillito, A. M., The pretectal light input to the pupilloconstrictor neurones, J. Physiol. (Lond.), 204 (1969) 36-37. 13 Sillito, A. M. and Zbrozyna, A. W., The activity characteristics of the pregangliomc pupllloconstrictor neurones, J. Physiol. (Lond.) 211 (1970) 767-779 14 Siminoff, R., Schwassmann, H. and Kruger, L., Unit analysis of the pretectal nuclear group in the rat, J. comp. Neurol., 130 (1967) 329-342. 15 Stone, J. and Fukuda, Y., Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells, J. Neurophysiol., 37 (1974) 722-748.