May 15, 1989 - concave and could swing aside, thus covering 180" of the visual field. As reference points, positions of the Areae centrales on the screen were.
ACTA NEUROBIOL.
EXP. 1989, 49: 311-325
THE INHIBITORY COMPONENTS IN THE RESPONSES OF THE LATERAL SUPRASYLVIAN AREA NEURONS TO MOVING STIMULI IN CATS B. A. HARUTIUNIAN-KOZAK', R. L. DJAVADIAN', A. ,A. HEKIMIAN1 and K. TURLEJSKI I Institute of Expdanenkal Biology, Armenialn Academy of Sciences, 7 Asratyan St., 375044 Erevan, USSR and =Nencki Institute of Experimental Biology, 3 Pasteur St., 02-093 Warsaw, Poland
Key words: neuron, receptive field, inhibitory component, discharge region, suprasylvian area
Abstract. The inhibitory components in the neuronal responses of the cat's lateral suprasylvian area (LSA) to moving bright and dark stimuli were investigated. The LSA neurons could be divided into two groups. Neurons of the first group (33°/oi) do not reveal spatial displacement of the inhibitory zones and show displacement of the discharge centers in the receptive field only for one polarity of contrast of mwing stimuli, either brighter or darker than the background. The second group (67O/m) contained the neurons which showed a spatial displacement of the inhibitory components and discharge centers in the receptive field for either polarity of contrasts of the moving stimuli. Tested with stationary flashing stimuli, the majority of neurons in both groups had overlapping ON-OFF discharge regions within their receptive fields. The results obtained with moving stimuli of different speeds and with the masking method suggest the rebound origin of the inhibitory responses m LSA neurons. INTRODUCTION
The suprasylvian area (LSA) of the cat's cortex presumably plays an important role in the central processing of visual information. It receives afferents from both the geniculostriate (19, 25, 26, 32, 37, 38)
and the extrageniculate structures (2, 14, 28, 29, 33). The LSA neurons seem to be engaged mainly in the analysis of mwing patterns. They respond vigorously to moving stimuli and mlany of them reveal the property of directional sensitivity (4, 5, 18, 24, 34, 39, 41, 42). We have previously show (16) that there are clear-cut inhibitory components in the responses of numerous LSA neurons to different types of moving visual stimuli. A well known explanation of the mechanisms of inhibitory responses in the visually sensitive neurons of geniculostriate structures is based on the polarity of contrast of stimulus (brighter or darker than the background) and the existence in the receptive fields of discrete zones with ON alnd OFF properties (27, 35, 36). But this explanation can not be applied to the LSA neurons. Most of the LSA neurons have receptive fields with overlapping ON and OFF discharge zones. They reveal a rather weak correlation between static and dynamic properties of their receptive fields (15, 39). The investigation of the inhibitory components in the LSA neurons' responses to moving stimuli might contribute to understanding of the mechanisms of central processing of visual information by the LSA and shed some light on the functional differences between the geniculostriate and extrageniculate visual structures. In the present study we have examined the inhibitory processes of LSA neurons using moving and stationary bright snd dark stimuli. METHODS
Thirty five adult cats weighing 2.5-3.5 kg were used. The b r a n stem was transected at the pretrigeminal level under ether anesthesia, which was immediately discontinued after the transection (1, 44). The skull was trephined and the opening that exposed the LSA was filled with 3010~agar in 0.9D/rNaCl solution. All pressure points and wounds on the head were injected with Novocain (5Vo). The cats were paralysed with an intramuscular injection of the myorelaxant Ditilin (dijdide dicholine esther of succinic acid, 7 mglkg) and artificially respired (19 strokes/min, stroke volume 20 ml/kg of body weight). The pupils were dilated with topical application of O.l'O/u Atropine solution and the corneas were protected from drying with zero power contact lenses. Nictitating membranes were retracted by instilling lQ/uneosynephrine into the conjun~ctivalsac. Spectacle lenses were used to focus the eyes on the screen. Arterial blood pressure, heart rate and electroencephalogram were constantly monitored. The blood pressure remained at the 90-100 mm Hg level and the heart rate at 130-150lmin. The electroencephalogram monitoring showed that the preparation re-
mained constantly awake. Throughout the experiment the body temperature was kept at 38' C with a heating pad. Single unit activity from PLMS area was recorded with tungsten microelect~odes(23). Poststimulus time histograms (PSTH) of responses to moving and stationary stimuli were computed. We used a 2 s time base (bin width 4 ms) a d repeated the stimulation cycle 16 times for each histogram. The base-to-base histognams were prepared in a manner slightly diffe~entfrom the one proposed by Emerson and Gerstein (10, 11). Two high sensitivity photodiodes were placed on the screen on the previously established borders of the receptive field. Each photodiode emitted an electric pulse when the edge of the stimulus (bright or dark) was passing through it. The pulse was fed into the analyser via a Schmitt trigger so that the maximally filled bins of the histogram provided reference points for the synchronization of the starting and ending moments of the s p t ' s motion. These precise markers allowed for the base-to-base matching of the PSTH's, with the upper part of the figure showing the neuronal responses to movement in one direction and the lower to movement in the opposite direction. Receptive fields of the neurons were plotted on the projection screen situated 1 m from the nodal points of the cat's eyes. The screen was concave and could swing aside, thus covering 180" of the visual field. As reference points, positions of the Areae centrales on the screen were plotted using the method of Fernald and Chase (12). The units were stimulated with bright and dark spots 3-5' in diameter moving with an angular velocity of 40-60'1s. In all experiments the luminace of the bright spots was 8 lx against 2 lx background, that of the dark spots was the converse, 2 lx against 8 lx back-ground, and the contrasts of light and dark spots were adjusted to be equal. The stimuli were moved with a mirror-galvanometer system driven by a trapezoidal waveform generator. Stationary properties of the neuron's receptive fields were outlined by stationary flashing bright spots positioned successively throughout the receptive field. We have shown previously that some neurons in LSA respond preferentially to moving dark stimuli rather than to bright ones (7, 18). Thus, it seemed to be more appropriate to investigate the static properties of their receptive fields also by stationary flashing dark spots. Figure 1 illustrates our method of delivering these. Two projectors (one for the dark, another for the bright spots) were arranged so that the images projected through them were precisely superimposed. A shutter driven by a pulse generator at a frequency of 11s was mounted in the projector that delivered the bright spot. The dark spot was shining constantly on the screen. When it was opened, the bright spot increased the luminance
of the dark spot to 8 lx, making it equal to the luminance of the background. This was called "dark OFF" because of the disappearance of the dark spot from the visual field. When the shutter on the bright projector was closed, the dark spot reappeared on the screen and this was called "dark O N . Dark off
Dark on
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Fig. 1. Schematic representation of the principles of obtaining stationary flashing dark spots. D, dark spot projector; B, bright spot projector.
In some experiments a visual field masking method for moving stimuli was used (see ref. 13). For this purpose, slides with bright strips of different sizes were prepared. When they were projected on the screen, the whole visual field was darkened except for the light strip, and the visible movement of the spot was limited by the strip's width. At the end of the experiment an electrolytic lesion (10 PA for 5 s, active electrode negative) was made at the recording point. Then the animal was deeply anesthetized with i/v injection of penthobarbitone sodium and perfused through the arteria carotis with physiological saline followed by 10o/cw formaline solution. The electrode track was reconstructed from 30 pm histological sections that were cut after fixation of the brain for a week in 10Q/(rformalin solution. RESULTS
Data from 115 PLMS neurons were collected. The sizes of LSA neuron receptive fields varied from 10 to 2,000 deg2. Neurons with large receptive fields as a rule responded to the moving stimuli "smoothly", i.e. with an excitation with no visible inhibitory components. Inhibitory components in the responses were observed mainly in neurons with relati-
vely small receptive fields (10 to 300 deg2). The majority of the small receptive fields were located near the Areae centrales. Most of these neurons had a high level of spontaneous activity which decreased or disappeared during inhibition. Thus, it was possible to identify the inhibitory components of responses without monocular conditioning (3, 2 1). All neurons showed a clear-cut inhibition of spontaneous discharges occurring before or after the excitatory response to the visual stimuli moving across their receptive fields. At the first step in the exploration of the receptive fields, we applied movements of dark and bright spots along the full length of the horizontal axis of the field. The movement d the spot evoked excitatory responses that had one or two, rarely more, peaks (discharge centers) and symmetrically or asymmetrically located inhibitory zones around these peaks. Changes in the direction of movement elicited displacements of spatial localizations of the discharge centers as well as adjacent inhibitory components in the receptive fields. The mode of these displacements usually also depended on the polarity of the stimulus contrast. Further, there were individual variations of these displacements for different neurons. On these bases neurons were classified into two groups.
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g is' Fig. 2. Responses of a neuron in which spatial localization of discharge regions and inhibitory zones in the receptive field changed for the opposite direction of movement of a bright spot. A, base-to-base PSTH of responses to a bright spot moving along the horizontal axis of the receptive field. B, base-to-base PSTH of responses of the same neuron to a moving dark spot. C, the PSTH of responses to a stationary flashing bright spot positioned subsequently at nine test-zones of the receptive field along the horizontal axis. RF, receptive field. Numbers at the top of histograms indicate the test-zones of the receptive field subsequently explored by stationary flashing spot shown in receptive field. The size of moving spots: 5'; flashing spot: 3'; bin width: 4 ms. Arrows indicate the directions of movement. These explanations are also valid for the next figures. 2
- Acta Neurobiol. Exp. 6189
In the first group we included neurons showing spatial displacement of discharge regions in their receptive fields only for one of the pair of the corresponding stimuli - bright or dark. Those neurons constituted 33O/u of our sample (38 neurons). A moving spot of the same size and shape, but with reversed polarity of contrast did not change the spatial localization of the discharge regions in the receptive field of these neurons. Responses of one of these neurons are shown in Fig. 2. The spatial location of the discharge region and that of the inhibitory zone in the receptive field was different for opposite directions of movement of the bright spot (Fig. 2A). During the movement from left to right the spontaneous discharges were inhibited when the stimulus was crossing the left part of the receptive field and the excitatory response was evoked from the right side of the receptive field (Fig. 2A, the upper part of the histogram). The movement to the left (Fig. 2A, lower part of the histogram) evoked just the opposite response: the right subregion of the receptive field which had given an excitatory response (for the opposite direction of movement) was now inhibiting the spontaneous discharges of the cell, and the left subregion gave an excitatory response instead. Thus, the opposite directions of bright spot movements resulted in different spatial localizations of the discharge region and adjacent inhibitory zone. By contrast, the dark spot moving across the receptive field of the same neuron evoked an excitatory response with zones of inhibition positioned symmetrically on both sides of the excitatory peak of the response. There was no spatial displacement of the discharge region when the direction of movement was changed (Fig. 2B). When tested with the bright stationary flashing spot, the overlapping ON-OFF discharge regions witK dominating OFF-responses were revealed (Fig. 2C). Even the lateral region of the receptive field that generated a clearly inhibitory response during the movement of the dark stimuli produced OFF-ON phasic responses to flashing spots and not the pure ON response, which one would expect to be the basis of the inhibitory responses to the moving dark stimuli (Fig. 2C, responses 1-3 and 6-8). Thus we could not find any spatial correlation between the inhibitory responses elicited by the moving stimuli and the static organization of the receptive field revealed by the responses of the cell to the stationary flashing stimuli. In other neurons of this group we found the reverse phenomenon: spatial displacement of the discharge region was observed when the dark spot moved across the receptive field and the location of the region was stable when the bright spot was used. The neuron presented in Fig. 3 has a receptive field with a sandwich-like organisation, resembling that of the simple cells in the striate cortex. A moving bright spot reveals two discharge centers of the receptive field with the inhibitory compo-
nents almost symn~etricallyarranged around them (Fig. 3A). As could be seen from the figure, the static locations of the discharge regions as well as the corresponding inhibitory components are stable and did not change during two opposite directions of movement. By contrast, the
Fig. 3. Responses of a neuron with spatially stable location of the inhibitory zones in the receptive field for the movement of a bright spot. A, base-to-base PSTH of responses to a bright spot moving along the horizontal axis of the receptive field. B, base-to-base PSTH of responses to a moving dark spot. C, responses to the flashing bright spot positioned side-by-side in three test-zones of the receptive field.
dark spot reveals one discharge region with an asymmetrically located inhibitory regions and these locations depended on the direction of motion (Fig. 3B). A stationary flashing bright spot positioned sequentially along the horizontal axis of the receptive field revealed an ON-region in the center (Fig. 3C, response 2) and two OFF-regions (Fig. 3C, responses 1 and 3). Judging by the static structure of the field, there should be, at least during the movement of the bright spot, a symmetrical inhibition around the only discharge region. However, the inhibitory components are located rather asymmetrically in the response, intermingled between two discharge centers. By contrast the moving dark spot which should have elicited the discharges in two separate OFF flanks of the field, reveals a single discharge region with asymmetrically arranged inhibition (Fig. 3B). Thus, the static structure of receptive field could not provide a full explanation of the dynamic properties of the neuron. The second group consisted of the neurons which showed spatial displacement of the discharge regions and inhibitory zones in their receptive fields for both the bright and dark moving spots. This group constituted 67Vu (77 neurons) of our sample of LSA neurons. The responses of a neuron presented in Fig. 4 are typical for this group. It is apparent from the figure that the discharge regions were spatially displaced du-
ring the two opposite directions of movement of dark or bright spots and corresponding inhibitory components of the response undergo similar change in spatial location (Fig. 4A and B). The static properties of the receptive field of this neuron were thoroughly explored by stationary flashing dark and bright spots. The PTS histograms of responses to sti-
Fig. 4. Response of a neuron with spatially unstable localizations of inhibitory zones in the receptive field a t the motion of dark and bright spots. A, B, base-tobase PSTH of responses of the neuron for moving dark and bright stimuli. C, D, responses of the same neuron to dark and bright stationary spots positioned succesively along the horizontal axis of the receptive field. Note the absence of the reaction to the stationary stimulation.
muli positioned in three test zones in the receptive field are presented in Fig. 4C and D. The neuron did not respond at all to either stationary stimulus. As could be seen from the figure, neither the dark nor the bright spot elicited clear-cut changes in the cell firing rate. Thus, it should be concluded that the spatial displacement in the responses of the presented neuron coud not be explained on the basis of asymmetries in the static profile of the receptive field. Subsequently, we tried to find in the receptive fields of investigated neurons the spatial correlates of inhibitory responses using moving spots rather than stationary stimuli. The responses of a neuron with the inhibitory effects evoked by the movement of the dark spot are presented in Fig. 5. The upper histogram in Fig. 5A shows neuronal responses for stimulus moving from right to left and the lower one the responses for the left-to-right direction. In both cases the movement of a dark spot evoked an inhibitory response followed by an excitatory peak, independently of the direction from which the spot entered the receptive field (Fig. 5A). We have also tested the responses of this cell with movements of a small amplitude (lo), limited to the region of receptive field supposed to be inhibitory for the appropriated direction of the motion. The tests did not reveal any inhibitory zones. In both the left the right re-
gions of the receptive field dark spot motion elicited feeble excitatory responses when the spot was leaving the receptive field (Fig. 5B and C). With movements of small amplitude we could not evoke any response from the subregions of the receptive field that seemed to be inhibitory when tested with the motion of the large amplitude.
Fig. 5. Responses of a cell to the small amplitude of movements of the dark spot within the test-zones of the receptive field. A, base-to-base PSTH of the neuron's responses to a moving dark spot along the entire length of the horizontal axis of the receptive field in two opposite directions of motion. B, responses of the same neuron to a small amplitude of movements of a dark spot in the left subregion of the receptive field. C, responses of the neuron to the small amplitude of movements of the dark spot in the right subregion of the receptive field.
Thus, we could never find an appropriate spatial zone in the receptive field which would unequivocally coincide with the zone from which the inhibitory response was elicited by the moving stimulus. Probably there is some other non-spatial mechanism organizing the inhibitory response of the cell. The reason for the lack of the response to the motion of small amplitude could be that such a small amplitude of dark spot movement is insufficient (subtreshold) for triggering the inhibitory mechanisms of the cell. In the next group of experiments stimuli moving with different speeds were applied to determine whether the speed of motion and ternporal factors had any influence on the inhibitory component of the response. The results of one such experiment are presented in Fig. 6. The dark spot was moved along the horizontal axis of the receptive field of the neuron. Only one drection, left-to-right, of stimulus motion is presented in the figure. It is seen from the figure that the inhibitory component in response to the 20°/s movement is well pronounced (Fig. 6A),
while the inhibitory component in response to the 5"/s and 2.5"/s movements are clearly weaker (Fig. 6B and C). At the speed of 1.3"/s or 1°/s the inhibitory components disappear (Fig. 6D and E). It appears therefore that the temporal rather than spatial factors may be crucial for the organisation of the inhibitory responses of the LSA cells. The velocity tests in conjunction with the lack of the spatial correlates of inhibitory components in the receptive fields suggested to us that the inhibitory component in the response of LSA cells represent a rebound after-effect of the initial excitation of the neuron.
Fig. 6. Responses of a neuron to different speeds of movement of the dark spot along the horizontal axis of the receptive field. A-E, responses of the neuron to a moving dark spot in the left-to-right direction. The inhibitory component of the response disappeared at low speed of movement (1.3-1.0's).
To test further this suggestion we applied the masking technique (13) in the experiments presented below. The sizes of the receptive fields of the cells under investigation were estimated using a hand-held dark stimulus. The size of the receptive field of the neuron presented in Fig. 7 was 6" horizontally ad 6" vertically. The response of the cell to the dark spot moving along the entire length of the horizontal axis was recorded (Fig. 7A). It had two inhibitory components, both before and after the excitatory phase. The flashing light spot positioned in the center of the receptive field elicited an OFF response (Fig. 7B). Afterwards the entire receptive field was masked and a 3" window was located at the left border of the receptive field. The dark spot moved to and fro within the limits of the window. No response was evoked from this area (Fig. 7 C-1). Then the window was placed on the right side of the receptive field and the same procedure was repeated. Again there was no response (Fig. 7 C-2). Finally the window was positioned over the left half of
the receptive field. Again, the amplitude of movement of the dark spot was equivalent to the window's width, i.e. 3O (Fig. 7 C-3), since the remaining visual field was masked. In this case, however, clear cut discharges of the cell were elicited together with the inhibitory component. Then the window was shifted to the right half of the receptive field and
Fig. 7. Responses of a neuron to moving and stationary stimuli, when using the masking method. A, responses of the neuron to a moving dark spot along the horizontal axis of the receptive field. B, responses of the same neuron to a stationary flashing light spot positioned in the center d the receptive field. C, 1,2 responses of the neuron to a moving dark spot (amplitude of the movement 3O). The whole visual field is masked (darkened), except for the window of 3 O width placed outside, adjacent to the left and right borders of the receptive field. C, 3,4 responses to a 3' amplitude of movement of the dark spot in the left and right subregions within the receptive field. The rest of the visual field besides of window space is darkened (masked).
the movement was pelrformed again (Fig. 7 C-4). As can be seen from the figure, the response is the same as that presented in Fig. 7 C-3. When we measured the duration of the response at the PST histogram and its spatial correlate in the receptive field, we found that the response (the excitatory and inhibitory components together) would last so long that in that time the stimulus would have travelled a distance of more than 5". There is, however, no doubt that the stimulus moved only w:thin the space of 3". Thus, the inhibitory phase of the response produces the extra response duration which is seen in the PST histogram. Thus again, these results are consistent with our suggestions that the inhibitory phase of these cells response represents an after-effect following the primary excitation of the neuron.
DISCUSSION
The inhibitory phase in the responses of most of the retinal ganglion cells or geniculate neurons to dark and bright moving stimuli is related to the concentric organization of their receptive fields. Indeed there is close correlation between the static and dynamic organization of the receptive field of these neurons (27, 35, 36). In simple neurons of the cat striate cortex there is also a clear-cut correlation between the static and dynamic properties of their receptive fields (10, 30). Thus, the inhibitory components in the responses evoked by moving stimuli have spatial correlates in the receptive fields, although some authors (20, 31, 43) could not find strict correlation between the dynamic and static properties of simple cells in striate cortex. The neurons of M A generally show poor correlation between the static and dynamic properties (15). It was most striking that the asymmetrical inhibition frequently observed in the responses of the LSA neurons to moving stimuli did not correlate spatially with the static organisation of the receptive fields, even when they consisted of two spatially distinct ON and OFF zones. Thus, the inhibitory subregions of the receptive fields could be easily revealed with moving stimuli that evoked clear-cut inhibition of the cell's spontaneous discharges. However, when tested by stationary dark or bright spots, the same spatial subregions of the receptive field which were inhibitory during movement as a rule gave mixed ON-OFF responses to the stationary flashing spots. A detailed analysis of the inhibitory components in the responses of the LSA neurons indicated that even when a spatial region, with inhibitory properties could be pinpointed within the receptive field, the small amplitude movements of a spot in that presumed inhibitory zone evoked only weak excitatory responses and never an inhibition of the spontaneous activity of the neuron under investigation. Thus, the mechanisms underlying the inhibitory components of responses of LSA neurons to the movement are not related to the static pattern of organization within the receptive fields. Small amplitude of motion seems to be insufficient to evoke any noticeable after-effect of preceding weak excitation. The disappearance of the inhibitory component from the neuronal responses at very slow velocities of movement (Fig. 5) could be due to the relatively weak response to slow motion as described by Creed et al. (6) for spinal cord neurons. Presumably such a weak response is not followed by postexcitatory reduction in firing rate. So these data support, to some extent, the rebound mechanism hypothesis. Furthermore, the masking method used in the experiment presented in Fig. 7 indicates that the inhibitory phases in the responses of these cells to moving stimuli have the
characteristics of temporal after-effects. Since the receptive field of the neuron studied appeared to be homogenous and contained only OFF discharge region, a dark spot crossing the receptive field should evoke excitatory responses only. Thus, the inhibitory component following the discharge seems to be a rebound reaction after the cells discharge. Such a rebound mechanism probably accentuates the peak responses of the cell to the applied stimuli as well as helping to specify the spatial location of the moving object in the visual field. One more feature of LSA neurons distinguishes them from the neurons in other parts of the visual pathway. For example, Dreher and Hoffmann (8, 22), when studying the spatial organization of the receptive fields of collicular neurons (structures which project via lateral posterior pulvinar complex to LSA area - cf. 33) they stated that a moving stimulus elicits its maximal response from the same position in the receptive field for different directionse of stimulus movement. Thus, the location of the discharge region in the receptive field of collicular neurons was shown to be stable. By contrast, we have shown that the discharge regions of the receptive field of the LSA neurons could be displaced spatially depending on the direction and polarity of contrast of the applied moving stimuli. This mechanism could play an additional role in the central processing of information about contrast and the direction of movement of visual stimuli.
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