EFFECTS OF BACKGROUND ILLUMINATION ON VISUALLY EVOKED RESPONSES OF NEURONS IN THE CLARE-BISHOP AREA OF THE CAT

Transcription

1 ACTA NEUROBIOL. EXP. 1981, 41: EFFECTS OF BACKGROUND ILLUMINATION ON VISUALLY EVOKED RESPONSES OF NEURONS IN THE CLARE-BISHOP AREA OF THE CAT B. A. HARUTIUNIAN-KOZAK, D. K. KHACHVANKIAN and R. L. DYAVADIAN Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR Orbeli 22, Erevan , USSR Key words: multimodal discharge, direction selectivity, background illumination Abstract. Functional properties of visually driven neurons were investigated at various levels of background illumination. Roughly 50 /o of the investigated cells inhibited their responses to stationary flash lights after background illumination, about 25O/o did not show any difference and 25O/o were facilitated. The increase of the background illumination influenced the movement evoked responses in various ways. The activity of 42O/o cells of this group was inhibited by an illumination of the background and 19O/o of cells revealed a facilitation of their responses. Abut half of the cells changed their directionally sensitive responses into direction non-sensitive ones and 35O/o did the opposite. Seventy one percent of multimodal neurons lost their response multimodality, whereas 140/0 of them preserved this property during the background illumination. INTRODUCTION Numerous investigations carried out with single unit recordings (4, 6, 8, 9, 15-17) have indicated that the neurons of the lateral suprasylvian area {Clare-Bishop area) of the cat are sensitive to moving visual stimuli. We have confirmed these data in our earlier investigations (4, 8, 9) and reported additional observaticms on the sensitivity of the Clare-Bishop area neurons to the stationary flashing lights (8). In this study we present results concerning the effects of background illumination on the

2 responses of the cells in the Clare-Bishop area to stationary and moving visual stimuli. Modulatory influences of background illumination on the responses of visually-driven neurons were described by many authors (1, 10, 11, 14). Those investigations concerned mainly the geniculostriate but almost never the associative visual structures. The PIPsent study is, to our best knowledge, the first attempt to investigate the modulatory effects of background illumination on the activity of visually sensitive neurons in the associative lateral suprasylviaa area. METHODS The experimental method was described in detail in a previous study (4). Tracheotomy, cannulations of jugular veins, carotid and femoral arteries were done under ether anesthesia. The head of the animal was fixed in the stereotaxic apparatus (Horsley-Clarke, modified for visual research). Pretrigeminal brain stem section was performled (2,18) and then the animal was artificially ventilated (19 strokes/min, stroke volume 20 mlkg of body weight). Ditilin (diiodide dicholine esther of succinic acid) was administred for immobilisation (7 mgkg every hour). A portion of the skull overlying the suprasylviian gyrus was surgically removed. The exposed dura was cut and reflected and a mixture of 3O/o agar in physiological saline was placed on the brain. The body temperature was kept at 38OC by a thermostatic pad. EEG and heart activity was monitored continuosly. Arterial blood pressure was ocassionally monitored and found to be stable at about mmhg. Pupils were dilated with O.lO/o atropine sulfate and nictitating membranles removed surgically. The corneas were protected by "0" power contact lenses. Occassionally the refractive error of the eyes was measured and appropriate lenses used. No differences in reactions of the cells with or without these corrective lenses have been observed. The main experiments were done without corrections of the refractive error. Light spots of different sizes (1-20') were projected on to a concave screen situated in front of the cat's eyes at 78 cm distance from the nodal points. The intensity of the light spot illumination ranged between 1 and 100 Ix, the background illumination to 10 lx. The velocities of movement of the light stimuli were 100 to 180 /s. Flashing 13ght spots (500 ms - light, 500 ms - darkness) were used as stationary stimuli. The times for light and dark adaptation were 15 and 40 min consecuently. Recordings of the single unit activity were performed using tungsten microelectrodes (5). Action potentials were averaged by an interspike interval analyzer (7). Each action potential was displayed as a dot on

3 the oscilloscope screen. The abscissae of Figures (1-9) show the time of stimulation, the ordinatte - the interspike intervals. Averaging was achieved by superposition of the unit responses to 15 repetitions of stimuli. Formalin-saline perfusion of the brain was performed routinely after each experiment and the electrode track position was histologically verified. RESULTS Neuronal responses evoked by the stationary flashing light In the first series of experiments the effects of different levels of background illumination on the neuron responses to stationary flashing light were investigated. Responses evoked by a light spot positioned in the center of the neuron's reoeptive field were analysed. The reason for Fig. 1. Inhibitory effects of the background illumination on the neuronal responses evoked by a stationary flashing light spot positioned in the center of the receptive field. A, C, responses of two on-off neurons in the dark. B, D, responses of the same neurons during a 5 lx background illumination. E, response of an on neuron in the dark. F, response of the same neuron during a 1 lx background illumination. Ordinates indicate the interspike intervals, abscissae-the time of stimulation. The black strips at the bottom of the figure mean light-off, and the white stripslight-on. The diameter of the light spot is 5". The numbers on each frame indicate the luminances of stimuli (st) and background illumination. Responses to 15 stimuli were superimposed for the purpose of averaging. Explanations are the same for the following figures.

4 this was the fact that during dark adaptation changes in the responses of the receptive field periphery were conditioned by scattered light. A general classification according to the pattern of neuronal responses to the flashing light in darkness showed that of the 103 neurons investigated 79 reveal monomodal distribution of discharges and 24 multimodal distribution of the neuronal spikes. Among 79 neurons with monomodal responses 40 were on-off, 25-off and 14-on. Of 24 neurons with the multimodal type of responses 13 were on-off, 7-off and 4-on. A suppression of the spike discharges is the most prominent influence of background illumination on the evoked responses of the neurons. The spike activity of 57.2"o of all neurons observed was inhibited by the background illumination. Figure 1 illustrates the examples of neuronal responses which reveal the suppression effect. Figure 1A demonstrates the responses of a cell to the stationary flashing spot in semidarkness (background illumination lx). There is an on-off response. Increasing the intensity of the background illumination results in the suppression of the cell activity (Fig. 1B). The second neuron presented on the Fig. lc, D loses its clear-cut response elicited in the dark (Fig. 1C) when the background is illuminated (Fig. ID). The third neuron on Fig. le, F is an on neuron which also suppressed its activity after illumination of the background. 22.3OIo of all neurons revealed a facilitation by increasing the number of discharges during light adaptation. The on-off St 40L ms A Backg illurn 0.1L 100 St l0l C Backg illum 0.1 L 1000 Fig. 2. Facilitatory effects of the background illumination on the neuronal responses evoked by a stationary flashing light spot. A, B, the responses of an off neuron in the dark (A) was transformed into a well defined on-off response during the background ill~m~ination (B). C, D, the responses of an on neuron in the dark (C) became facilitated during background illumination (D).

5 neuron of Fig. 2A, B which generated a weak response to the flashing light spot during semidarkness (Fig. 2A), increased th'e number of discharges during a light adaptation (Fig. 2B). In Fig. 2C, D a facilitation of the responses of an on neuron during background illumination is demonstrated. Fig. 2C represents the response of the cell to the flashing light spot in the dark, and Fig. 20, the respanse of the same neuron during a background illumination of 5 lx. As seen from the figure, a clear-cut facilitation of discharges occurs. The activity of 20.3OIo of neurons remained unchanged after turning the background illumination on. One of such neurons is presented in Fig. 3. Table I illustrates the above mentioned data analyzed quantitatively. Fig. 3. The responses of an on-off neuron in dark (A) did not change appreciably at different levels of the hackground illumination (B and C). Effects of background illumination on different types of neurons sensitive to stationary visual stimuli Types of Number Suppression Facilitation Unchanged neurons of neurons [941 [%I [%I -- off On Multimodal Neuronal responses evoked by "moving" stimuli Various effects of the background illumination on the responses of movement-sensitive neurons have been observed. A total of 91 neurons were investigated. 45 were directionally non-selective, 25 - directionally selective, 21 - multimodal. The following classification will characterize the effects observed in detail.

6 The first group (41.7OIo) includes neurons which suppress their movement induced activity or lose it during the background illumination. Figure 4 rep~sents examples of two neurons of this group. Figure 4A illustrates the response of a direction non-selective neuron to the movement of the light spot through its receptive field in the dark. As seen from the figure the response is well defined. The low level maintained activity makes the response accentuated and clear. Figure 4B represents 6 L st 5 Backg illum 1 L C Backg illurn 0.1 L St 12L D Backg illum 2 L Fig. 4. Inhibitory effects of the background illumination on the cell responses evoked by a moving light spot. A, C, responses of two directionally non-selective neurons to the movement of a light spot across their receptive fields in the dark. B, D, responses of the same neurons during background illumination. Arrows indicate the direction of the movement of the light spot. the responses of the same neuron to the moving light spot during background illumination of 1 lx. A severe suppression of spike discharges occurs. Another neuron in Fig. 4C, D which also has a well-defined response in the dark (Fig. 4C) loses its evoked activity during the background illumination (Fig. 40). At first it seems that the suppression effect of the background illumination was the result of the lowering of contrast between the stimulus and the background. Numerous neurons, however have been observed which, contrary to the previous group, elicit better responses i.e. facilitation effect at light adaptation, although the contrast of stimuli against the background had been lowered as well. These neurons constituted the second group (18.6O/o). The examples of neurons of this group were demonstrated in Fig. 5. All three neurons (Fig. 5A, D, G) reveal weak responses to the movement in darkness. When increasing the background illumination to 1 lx and 3-5 lx, the number of evoked discharges increased and the responses bacame more accentuated (Fig. 5B, E, H, C, F, I). In addition, the neuron of Fig. 5A

7 changes its preffered direction in darkness to the opposite one in light (compare Fig. 5A and B). The third neuron which had a weak response in dark with slight directionality (Fig. 5G) produces sharp directionally non-selective response in light (Fig. 51). As seen from the above-discus- St 10 St 15 A Backg illum0.1 L C Backg illum 3 L 10 L St D %ckg iilum 0.1 L.:. * ' * s' I 100. '.. St 16 1 Backg illum 4 L Fig. 5. Facilitatory effects of the background illumination on the movementevoked neuronal responses. A, D, G, responses of three different neurons to the moving light spot in the dark. B, E, H, responses of the same neurons during 1 lx background illumination. C, F, I, responses of the same neurons at higher levels of background illumination. sed figures, the background illumination apart of its quantitative effects (suppression or facilitation) can result in qualitative changes of the pattern of neuronal responses. Thus the third group includes the neurons which changed the characteristic patterns of their responses during the background illumination. Two neurons of this group are presented in Fig. 6. The neuron on Fig. 6A is moderately direction selective, generating some discharges to the movement of stimulus in the null direction when tested in dark, it was transformed into a purely direction selective one during light adaptation (Fig. 6B). The second neuron was directionally non-selective in dark, but it gives direction selective responses

8 during light adaptation (Fig. 6C, D). Figure 7. demonstrates examples of two neurons (Fig. 7A, C) which besides changing the preffered direction also accentuated their direction selectivity during background illumina- 10L st 11L ms A &kg illum 0.1 L I B Backg illum 1 L St 17L I D Backg illum 7L Fig. 6. Accentuation of directional selectivity of neurons during the background illumination. A, a response of a directionally selective neuron generating some discharges in the null direction (from right to left) is transformed into a purely direction-selective response during a 1 lx background illumination (B). C, the response of a directionally non-selective neuron to the movement of a light spot through its receptive field in the dark. D, the response of the same neuron became directionally selective during a 7 lx background illumination. st B Backg illum 1 1L 1L St D Backg illum.. 11L 1L Fig. 7. Accentuation and reversal of the directional selectivity of neurons during background illumination. A, C, responses of two different neurons to the moving light spot in the dark. B D, responses of the same neurons during a 1 Ix background illumination.

9 tion. The neuron in Fig. 7A responds vigorously in darkness to the motion of light spot through lts receptive field. Some preference to the motion from left to right is evident (Fig. 7A). After the background was illuminated (Fig. 7B), more discharges were elicited by the movement from right to left together with accentuation of the direction selectivity, (few discharges in the null direction). The neuron in the Fig. 7C, D completely inhibited its activity during movement of light spot in the null direction when the background was illuminated (Fig. 7C) whereas in darkness both directions of movement gave prominent responses. The 71.4OIo of multimodal neurons lost the characteristic multimodal distribution of discharges in the dark when the background was illuminated. Two examples of such neurons (Fig. 8A, D). show bimodal distri * St E Backs illum b ~ * h 16 1 L I... r.l St F Backa illum 16 5 L Fig. 8. Changes in the movement-induced responses of two bimodal neurons (A and D) at different levels of background illumination (B, E and C, F). Bimodal responses become monomodal. bution of evoked discharges to the two opposite directions of movement of light spot through their receptive fields. During background illumination of 1-2 lx (Fig. 8B, E) the bimodality disappeared. Further increases of background illumination (5 lx) did not result in any response changes (Fig. 8C, F). Nevertheless a small percentage of the multimodal neurons (14.2O/o) preserved their multimodality during the background illumination. For example the neuron presented on the Fig. 9A displayed trimodal responses to the movement of the light spot in the dark. During the illumination of the background (Fig. 9B) the trimodal pattern of the responses has been changed to bimodal. The seccmd neuron in the Fig. 9C reveals a bimodal response to the direction of movement from left to right, and monomodal response to the direction of movement from 8 - Acta Neurobiologiae Exp. 5/81

10 right to left (in the dark adaptation). At the background illumination of 1 lx the left-to-right directional response which was bimodal in the dark, now elicits a monomodal response and vice versa (Fig. 9D). The responses of the third neuron presented on the Fig. 9E, F are rare, for only two neurons of this type have been observed in the whole popula- Fig. 9. Neurons that retained their multimodality of responses to a moving light spot during 1 lx background illumination (B and D), as compared to those in the dark (A, C). E, a neuron which responded by a monomodal distribution of discharges in the dark and changed to a multimodal one during 1 Ix background illumination (F). ticm of neurons investigated. In the dark, the moving light spot elicits monomodal direction selective response of the neuron (Fig. 9E), during the background illumination of 1 lx the direction of movement from left to right which elicited monomodal responses in the dark evoked bimodal responses (Fig. 9F). About 10 /o of neurons did not change their activity evoked by moving stimuli either quantitatively or qualitatively during background illumination in comparison with that in the semidarkness. Table I1 represents a quantitative analysis of influences of the background illumination on the movement evoked responses of different types of neurons.

11 TABLE I1 Effects of background illumination on different types of neurons sensitive to moving visual stimuli. Types of Suppressed Facilitated Unchanged Transformed Transformed neurons [%I [%I [%I into into DS [%] non-ds [Oh] Direction non-sensitive Direction sensitive DISCUSSION According to some authors (11-14) the background illumination modifies the neuronal responses in the visual cortex. The same is true for the midbrain visual centers (3). To our best knowledge the Influences of the background illurninaton on the light induced activity of the lateral suprasylvian cortex associative neurons were never studied. The first conclusion which could be drawn on the basis of the experiments presented here is that the background illumination is less effective for the neuronal responses evoked by stationary stimuli in comparison with the movement evoked responses. The responses of the neurons evoked by stationary flashing light spots positioned in the center of the receptive field have not been changed at all during the background illumination in 25.3OIo of cases. Other neurons 48.3OIo showed the depression of their activity. The suppression effect is stronger in off neurons although some on neurons were inhibited during light adaptation. The activity of 26.4OIo of neurons (evoked by stationary light flashes) was facilitated after switching the background illumination on. The responses of neurons to the dynamic stimuli are modified in various ways by the background illumination. A clear-cut facilitation along with the suppression effects was observed in the responses of cells to the moving visual stimuli. These observations have much in common with those of Nunokawa (11) on visual cortex neurons. 12 of 25 neurons which responded preferentially to one direction of movement in dark (direction selective) lost their characteristic type of response during the background illumination and became directionally non-selective in the new conditions. Sixteen of 45 neurons, on the other hand, changed their pattern of activity from the direction non-selective one in the dark to the direction selective during the light adaptation. This

12 type of modulation of responses have been observed by Shevelev et al. (14) in the visual cortex. Multimodal responses evoked by moving stimuli in dark in a great majority of cases were transformed into monomodal ones during the background illumination. In an earlier study (4) we had suggested that the multimodal responses of cells may be concerned with the perception of size of the moving stimuli. Disappearance of the multimodal pattern of responses during light adaptation puts some doubt on this suggestion. But in some neurons the multimodality is resistant to the influences of the background illumination. It could be suggested that it were just these neurons that possesed the mechanism for the discrimination of stimulus sizes. The problem needs further and more detailed investigations. Integrating all the data concerning background illumination influences on the evoked activity of visually sensitive neurons we assume that visually driven neurons of associative areas of the brain are less sensitive to the levels of light adaptation while revealing mainly the general effects of suppression or facilitation of the discharges, and only a small percentage of neurons undergoes qualitative changes. REFERENCES 1. BARLOW, H. B., FITWUGH, R. and KUFFLER, S. W Change of organisation in the receptive fields of the cat's retina during dark adaptation. J. Physiol. (Lond.) 1'37: BATINI, C., MORUZZI, G., PALESTRINI, M., ROSSI, G. and ZANCHETTI A Effects of complete pontine transection on the sleep-wakefulness rhytm: the midpontine pretrigeminal preparation. Arch. Ital. Biol. 97: HARUTIUNIAN-KOZAK, B., WROBEL, A. and DEC, K The effects of background illumination on the responses of the neurons of the cat's superior colliculus to moving stimuli. Acta Neurobiol. Exp. 24: HARUTIUNIAN-KOZAK, B. A,, KHACHVANKIAN, D. K., OGANIAN A. S. and TUTUNDJIAN A. G Investigation of the neuron activity in the Clare-Bishop cortical area of the cat (in Russian). Neirofiziologia 10: HUBEL, D. H Tungsten microelectrodes for recording from single units. Science 125: HUBEL, D. H. WIESEL, T. N Visual area of the lateral suprasylvian gyrus (Clare-Bishop area) of the cat. J. Physiol. (Lond.) 202: HUXLEY, A. F. and PASCOE, J. E Reciprocal time-interval display unit. J. Physiol. (Lond.) 167: 4042P. 8. KHACHVANKIAN, D. K. and HARUTIUNIAN-KOZAK, B. A The properties of visually sensitive neurons in lateral suprasylvian area of the cat (in Russian). Dokl. Acad. Nauk Arm. SSR. 66: KHACHVANKIAN, D. K., BARSEGIAN, R. N. and HARUTIUNIAN-KOZAK, B. A The effects of background illumination on the responses of neurons of Clare-Bishop area to the moving visual stimuli (in Russian). Dokl. Acad. Nauk Arm. SSR 69:

13 10. KUFFLER, S. W Discharge patterns and functional organisation of mamalian retina. J. Neurophysiol. 16: NUNOKAWA, S Effects of background illumination on the receptive field organisation of single cortical cells in area 18 of the immobilized cats. Jap. J. Physiol. 23: SASAKI, H., BEAR, D. H. and ERVIN, F. R Quantitative characterisation of unit response in the visual system. Exp. Brain Res. 13: SASAKI, H., SAITO, Y., BEAR, D. H. and ERVIN, F. R Quantitative variation in striate receptive fields of cats as function of light and dark adaptation. Exp. Brain Res. 13: SHEVELEV, I. A Complete reconstruction of detector properties of cat's optic cortex neurons depending on the conditions of adaptation (inrussian). Dokl. Acad. Nauk SSSR. 217: SPEAR, P. D. and BAUMANN, T. P Receptive field characteristics of single neurons in lateral suprasylvian area of the cat. J. Neurophysiol. 38: TURLEJSKI, K Visual responses of neurons in the Clare-Bishop area of the cat. Acta Neurobiol. Exp. 35: WRIGHT, M. J Visual receptive fields of cells in a cortical area remote from the striate cortex in the cat. Nature 223: ZERNICKI, B Isolated cerebrum of midpontine pretrigeminal preparation: a review. Acta Neurobiol. Exp. 35: Accepted 5 May 1981