Activity of the striate cortex cells during saccadic eye movements of the alert cat

207

Ne,lroscience Research, 1 (1984) 207-222 Elsevier Scientific Publishers Ireland Ltd. NSR 00021

Research Reports

Activity of the Striate Cortex Cells During Saccadic Eye Movements of the Alert Cat Keisuke Toyama*, Minoru Kimura** and Yukio Komatsu Department of Physiolo~', Kyoto PrefecturalSchool of Medicine, Kawaramachi-Hirokoji,Kyoto 604 (Japan) (Received December 12th, 1983; Revised version received Februa~' 10th, 1984; Accepted March 7th, 1984)

Key words:eye-movement-related activity - visual cortex - simple cell- complex cell- saccadic suppression

SUMMARY Neuronal activity in the striate cortex was studied during eye movements of alert cats under reinforcement of eye movements with rewards of water. Striate cells were differentiated into two g o u p s exhibiting contrasting activities during and at intermissions ofsaccadic eye movements made in the presence o f a visual pattern: (1) saccade-excited (S E) cells (207/27 I) that were excited during saccadic eye movements and were much less active at intermissions; and (2) saccade-depressed (SD) cells (55/271) that were depressed during eye movements and were strongly active at intermissions. Under suppression of eye movements by retrobulbar paralysis or by withdrawal of the rewards, most SE-cells (89/104) exhibited photic responsiveness characteristic of"complex" cells in the anesthetized cat, and almost all SD-cells (23/26) that of"simple" cells. Therefore, it is likely that the two major neuronal populations in the striate cortex provide parallel channels of visual information which are gated in an alternative way during eye movements.

INTRODUCTION

A shift of the retinal image caused by passive movement of the eye produces a sensation of motion of the visual scene. Such an illusory motion of the visual scene never occurs during normal exploratory eye movements. It has been hypothesized that the visual scene is stabilized by subtracting the motor signals of eye movement (efference copy) from the reafferent retinal signals 11,32. Recent psychophysical studies demonstrated that the threshold for visual perception is elevated during movement of the retinal * Author for correspondence. ** Present address: Department of Physiology, Jichi Medical School, Minamikawachi, Tochigi, 329-04, Japan.

0168-0102/84/$03.00 © 1984 Elsevier Science Publishers Ireland Ltd.

208 image either due to the eye movement or due to movement of a visual stimulus 1s'2°'39. On the basis of these findings, another hypothesis is proposed that visual perception contains dual processes: perception of an image and evaluation of the coordinates of the perceived image in the visual space, operated in conjunction with the current eye movement21. Efforts have been devoted to establishing neuronal correlates to these hypotheses in the visual cortex of experimental animals. The results, however, have been rather controversial: In the monkey visual cortex, some results ~4'4° negated impingement of the motor signals of eye movements, while others2"5,I6 reported impingement of the inhibitory motor signals. Impingement of excitatory motor signals has been reported in the cat visual cortex26'z7. The main difficulties in these experiments have been to keep the animal fully alert and in motivating eye movements in darkness in a reproducible manner. In the present work, these difficulties were removed by operant control of eye movements29. Cats were deprived of water and their eye movements were controlled with rewards of water. Saccade-related activity of striate cells has been studied under reinforcement of eye movements with rewards of water, and was found to be related to photic responsiveness investigated under depression of eye movements by withdrawing the rewards, or under complete paralysis of eye movements by retrobulbar block 4. The results indicate that one population of striate cells, probably corresponding to the "simple" cells, is active at intermissions while the other population, corresponding to the "complex" cells, is active during the period of saccadic eye movements. A portion of the present results has been reported previously 17.

METHODS

Surgery Ten cats were used. Several days prior to the experiment preparatory surgery was performed under ketamine anesthesia (40 mg/kg). The surgery involved installation of (1) head holders and a recording chamber on the skull, and (2) two pairs of Ag-AgC1 electrodes: one pair at the upper and lower canti of the left orbit for electro-oculogram (EOG) recordings of vertical eye movement and the other pair at the temporal canti of both orbits for EOG of horizontal eye movement.

Training After recovery from surgery, each cat was deprived of water and trained to remain calm and quiet with their head fixed on the stereotaxic frame and to make saccadic eye movements. During the training, EOGs were monitored continuously and a reward (a drop of water, 0.05 ml) was given for every qualified eye movement (saccades larger than 10 ° in amplitude and faster than 40°/s in velocity). The cats quickly adapted to this experimental paradigm. Within a few days they willingly mounted the frame and performed saccadic eye movements as frequently as 60 times per minute under partial

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Photic stimulation The head of the animal was fixed on the frame, while its body and limbs were kept unrestrained. A tangent screen was placed in front of the animal (distance, 57 cm). T w o types of visual stimulators 35"3v were used to project patterned light stimuli (1-1.5 log unit brighter than background illumination of 4.5 cd/m2). One type of stimulator was equipped with a single rotatory mirror driven by a galvanometer and used for whole field presentation of various patterns, such as checkered (periodicity, 1-5°), striped (periodicity, 0.2-5 °), fine dot (grain size, 0.2-1 °) and visual noise (grain size, 0.2-1 °) pattern extending for the entire area of the tangent screen (200 cm x 150 cm). T h e other type of projector, with two rotatory mirrors and one electric shutter, was used for the presentation of light slits. Control signals were fed from a computer ( P D P 11/34) to the rotatory mirrors and

210 the electric shutter through a DA-converter. Adjustable parameters were shape (width, length and orientation), position and duration of presentation &stationary light slits a n d direction, amplitude, velocity and overall cycle time of moving slit stimuli. Moving light slits (velocity, 3-100°/s) were used to study photic responsiveness such as ocular preference, orientation, direction and length selectivities. Stationary light slits (0.2-2 ° wide and 3-20 ° long) were used to investigate internal structures of the receptive a r e a of striate cells. They were given randomly at 7-13 different positions in a receptive a r e a and peristimulus time histograms (PSTHs) of neuronal responses were constructed for 10-20 trials of stimulation at each stimulus position (at 1 Hz). This analysis could be done in a short period of time (within a few minutes) while eye movements were completely paralyzed by retrobulbar block or were temporarily suppressed by withdrawal of rewards (see above). Saccade-related activity of striate cells was studied either during presentation of the whole field stimuli or in absolute darkness. For studying saccade-related activity in darkness, both eyes of the animal were covered with sheets of black paper to ensure complete deprivation of visual input.

Recording Impulse discharges were recorded extracellularly from, cells in the striate cortex (1-5 mm posterior from the mid-frontal axis of the stereotaxic coordinates and a b o u t 1 mm lateral from the mid-sagittal axis) with a glass-coated stainless steel microelectrode ~4 while the cat was performing the trained task. The recording session, during which the task was partially reinforced, could be continued for a few hours. Between 4 and 10 cells were sampled in a single tracking, and electrolytic marking (10 #A tip positive for 1 min) was made for the last cell. The recording session was repeated o n c e a day and continued for about two weeks. Recordings were made from both sides o f the striate cortices with several markings in each cortex. The locations of the m a r k e d cells were determined histologically, and those of the other cells according to micromanipulator readings. Retrobulbar block In 5 of the 10 cats additional surgery was performed for retrobulbar block. T w o syringe needles (internal diameter, 0.3 ram) were stereotaxically inserted into both sides of the orbital fissures. Retrobulbar block was performed for the last cell in e a c h recording session by injecting a small amount (0.2-0.4 ml) of 10 ~o Xylocaine into each eye4. As monitored by the EOGs, eye movement was completely paralyzed almost immediately after the injection, and it was followed by complete mydriasis of both eye s, indicating that the ophthalmic nerves were completely blocked. As striate cells retained the same photic responsiveness as that before the block, the optic nerves appeared to remain intact. Complete paralysis of eye movement continued for 20-40 min and partial paralysis for another 20-40 rain.

211

Calibration of EOGs On the first day of the experiment, the EOGs were photographically calibrated. Under mesopic illuminations (4.5 cd/m2), which were used for presentation of visual stimuli, close-up pictures were photographed with a camera equipped with a telescopic lens (f = 135 mm) and an electro-magnetic shutter. Each of about 40 pictures of the right eye was taken from both lateral and frontal sides during intermissions of saccadic eye movements while the cat was performing the trained task. The photographic time sequence and EOGs were simultaneously monitored by a pen-recorder. The center of rotation of the vertical eye movements was determined in the superposed traces of the iris. Horizontal and vertical eye positions were determined in frontal pictures as angles of rotation of the right eye around the center of rotation. Amplitudes of horizontal and vertical EOGs were measured at each photographic time-frame, taking those corresponding to the first picture as the base-line. In order to eliminate errors in estimating vectors of eye movements due to incorrect orthogonality between the electrodes for horizontal and vertical EOGs, calibration was made by determining a matrix of constants (Axh, Axv, Ayh, Ayv) in the equation,

(I) which most optimally correlated amplitudes of horizontal and vertical EOGs (h and v) with horizontal and vertical eye positions (x and y). In most cats, Axv and Ayh were much smaller than Axh and Ayv (less than 10%), indicating that the electrodes for horizontal and vertical EOGs were practically orthogonal to each other. In all animals, the matrix was contstant over a wide range of eye positions (+_ 30 from the vertical and horizontal meridians of the visual field of the animal). The calibration during mesopic illumination was used for EOGs in darkness. Therefore, estimates of eye movements in darkness may contain some errors due to a change in calibration caused by different levels of illumination9. Calibration of EOGs was repeated once weekly.

Data processing Impulse discharges of striate cells were fed into the computer through a band-pass filter (tuned at 1 kHz) and a window discriminator, and the time of occurrence of impulse discharges was digitized by the computer (unit time, 0.1 ms). Amplitudes of horizontal and vertical EOGs were also digitized through an AD-converter (sampling time, 5 ms). The digitized data were stored on magnetic tapes for later processing. The data processing involved: (1) reconstruction of eye movements from the horizontal and vertical EOGs on the basis of equation 1 ; (2) determinations of parameters of saccadic eye movements, such as onset, duration, amplitude, velocity and direction; and (3) constructions of dot displays and average response histograms of impulse discharges synchronized at the onset of saccadic eye movements.

212 RESULTS

(I) Eye movement-related activity Two hundred and eighty-four cells were sampled from a region of the striate cortex. They were identified as cortical cells on the basis of their responsiveness to photic stimulation ~,t2"~3,3~'37.Their activity was studied in two experimental conditions: during presentation of a visual pattern, and in darkness. In the former condition, practically all cells (271/284) exhibited a change in spike activity in relationship to saccadic eye movements. In agreement with previous studies a6'27, a distinct dichotomy was found in their s accade-responsiveness: an excitation in one group of cells (S E-cells, 207/271), a depression in another group (SD-cells, 55/271), and an intermediate response in very few cells (9/271). Saccade-excited cells. During presentation of a checkered pattern, the saccadeexcited neurons (SE-cells) commonly discharged at a relatively low frequency (less than 10 impulses/s) in the absence of eye movements, and were briskly activated in conjunction with saccadic eye movements (Fig. 2A, dotted lines indicate onset of eye movements). A similar but less striking excitation occurred in absolute darkness (Fig. 2B). The saccade-related activity was studied by constructing a dot display (Fig. 3A) and an average response histogram (Fig. 3B), which lumped activities accompawing numerous saccadic eye movements of different amplitudes and directions (Fig. 3C). In the presence of a checkered pattern, saccade-excitation was commonly (126/167) composed of two components: an early excitation occurring during the eye movement (about 20 ms after the onset of the saccade, Table I) and a later component TABLE I RESPONSES OF STRIATE CELLS DURING SACCADIC EYE MOVEMENTS Figures in brackets indicate the number of cells studied. Cell type

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occurring at the end of the eye movement (about 80 ms) and lasting for an additional 150 ms (Table I). The saccade-excitation in darkness occurred with a longer latency and a shorter duration (Fig. 3 D - F and Table I) than that during presentation of a checkered pattern; it contained only a single component roughly corresponding to the later one of the saccade-excitation during presentation of a checkered pattern (cf. Fig. 3B and 3E). Therefore, it is likely that the initial component of the saccade-excitation is retinal in origin, possibly due to shifts of the retinal image of the checkered pattern during the eye movements, while the later component is extra-retinal in origin. The finding that a vast majority of the SE-cells exhibited saccade-excitation in darkness indicates that most SE-cells receive extra-retinal, as well as retinal, signals of eye movements. In 21 SE-cells, saccade-excitation was studied during presentation of various visual patterns. The retinal component of the saccade-excitation was equally prominent for all

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checkered, striped and visual noise patterns, and was therefore independent of the visual patterns. Saccade-depressed cells. The saccade-depressed (SD) cells maintained impulse discharges at a relatively high frequency (30-50 impulses/s) during presentation of a checkered pattern. Saccadic eye movement caused a transient depression of their impulse discharges (Fig. 4A). The tonic activity of the SD-cells was greatly reduced in darkness (less than 4 impulses/s), and consequently it was unclear whether saccadedepression was still present (Fig. 4B). A dot display and an average response histogram of the impulse discharges (Fig. 5A-C) showed that during presentation of a checkered pattern, saccade-depression occurred at approximately the same latency as that of saccade-excitation (Table I) and continued for the entire eye movement period (Table I). Subsequent to the depression, there was a slight rebound excitation lasting for a few hundred milliseconds. The saccade-depression was scarcely detectable in darkness (Fig. 5D-F). This abolition of saccade-depression in darkness occurred in all SD-cells, suggesting that saccade-depression is entirely retinal in origin.

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Intermediate cells. A few cells (n = 9) exhibiting an initial brief excitation and a later depression were classified as intermediate cells. (2) Photie responsiveness In 22 of the 135 cells whose photic responsiveness to photic stimulation was studied under retrobulbar paralysis which selectively blocked innervation of the extra-ocular muscles without affecting the optic nerves. The paralysis of eye movements continued for more than 20 rain. As examined by projection retinoscopy3, drifts of the eye position were smaller than 0.3°/h, which was as good as the stabilization of the eyes obtained under paralysis with a muscle relaxant 6. Under the retrobulbar paralysis, photic responsiveness, such as ocular and directional preferences and the orientation, length and velocity tunings, and the internal structure of their receptive fields was studied with moving or stationary stimuli presented by the computer-controlled projector.

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Additional cells (n = 113) were studied under transient stabilization of eye movements caused by withdrawal of the rewards for saccadic eye movements. In these cells, the ocular and orientation preferences were roughly determined with hand-moved light stimuli, and internal structures of the receptive fields and velocity tuning were quickly studied with computer-controlled light stimuli. About one-fifth of the cells (24/135) exhibited a relatively narrow receptive field (0.3-5°). Presentation of a stationary light slit in a region of the receptive field (position c in Fig. 6A) produced an ON response (Fig. 6C), while an O F F response (Fig. 6D) was obtained in another region (position d). Therefore, the receptive field was composed of two sub-areas adjoining each other, one producing the O N response (stippled area in Fig. 6A) and the other producing the O F F response (hatched area)• These ceils also produced a short burst of impulses when a light slit moved across the border of the ON and OFF response areas (Fig. 6B). The excitatory response area was frequently bonded with areas of side band inhibition, which was not quite clear in the case of Fig. 6B. They responded most optimally to a light stimulus moving at a relatively low velocity (less than 20 °/s). All of these response properties match the characteristics of the "simple" cells 1,12,13,19.31,33,37. Most of the remaining cells (91/135) exhibited a relatively large receptive field (2-14°). In most parts of the receptive field (positions c and d in Fig. 7A), a stationary light slit produced an O N - O F F response (Fig. 7C and D). Hence, their receptive field

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Fig. 6. Photic responsiveness of a "simple" cell under retrobulbar paralysis. A: receptive field and stationary light slit exposed at two different positions (c and d). Stippled area, ON response area; hatched area, OFF area. B: peristimulus time (PST) histogram of responses to 15 trials of stimulation with moving light slit (velocity, 10°/s). Ordinate represents the number of impulses discharged during 15 trials of stimulation. C: response to 12 trials of stimulation with a stationary stimulus at position e. D: that to a stimulus at position d. All responses were obtained under paralysis of eye movement by retrobulbar block. Calibration bar of 2 s applies to B and that of 0.2 s to C and D. consisted of overlapping O N and O F F areas (Fig. 7A). These cells were strongly responsive to a moving light slit. They produced impulses whenever a light stimulus travelled across the receptive field (Fig. 7B). The optimal velocity of a moving stimulus was greater (20-100°/s) than that for the "simple" cells. Therefore, these cells seem to correspond to "complex" cells 12"13'19'37. The remaining ceils (20/135) exhibited either intermediate responsiveness between the "simple" and "complex" cells (10/135) or were poorly responsive to photic stimulation (10/135). Length selectivity was studied in 4 "simple" and 18 "complex" cells under retrobulbar paralysis of eye movements. One of the 4 "simple" cells and 4 of the 18 "complex" cells exhibited strong end-stop inhibition and were classified as "hypercomplex" cells with "simple"-like receptive fields and those with "complex"-like receptive fields, respectivelyT,15. Another 4 "complex" cells exhibiting a large receptive field and lacking length summation or end-stop inhibition were classified as special "complex" cells 7'28. The remaining 10 "complex" cells exhibiting length summation but no end-stop inhibition were classified as standard "complex" cells 7. Of the 135 cells whose responses were studied during both saccadic eye movements

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Fig. 7. Photicresponsivenessof a 'complex'cell under retrobulbar paralysis.A-D illustrate responses in the same way as in Fig.6A-D. Velocityof stimulusmovementin B, 80°/s. Number of trials is 25 and 12, in B and C-D, respectively.Calibration bar of 0.2 s is for all records. and photic stimulation, 104 were the SE-cells containing all categories of the "complex" cell family (10 standard "complex", 4 "hypercomplex" with "complex"-like receptive field, 4 special "complex" and 71 "complex" cells whose length selectivity was not studied), cells exhibiting intermediate responses between the "simple" and "complex" cells (n = 8), and poorly responsive cells (n = 7). By contrast, all SD-cells (n = 26) belonged to the "simple" cell family (22 "simple" cells and 1 "hypercomplex" cell with "simple"-like receptive field), except for a few poorly responsive cells (n = 3). Five intermediate cells exhibiting an initial excitation and a later depression contained 1 "simple", 2 "complex', and 2 cells with intermediate responsiveness between "simple" and "complex" cells.

(3) Cortical depth of location The cortical depth of the 97 SE-cells and 20 SD-cells was determined by histological examination, Practically all SD-cells (18/20 ceils) were confined to the granular layer except for a few exceptional cells (2/20) in the supragranular layer. The SE-cells, on the other hand, were concentrated in the supragranular layer (56/97 ceils), or in the infra-

219 granular layer (34/97), with relatively few in the granular layer (7/97). No significant difference was found between the supra- and infragranular ceils in the amplitude of saccade-excitation (Table I).

DISCUSSION

Saccade-related activity of the striate cells The present study has demonstrated a distinct dichotomy occurring in the activity of striate cells during saccadic eye movements. When a visual pattern was presented to the animal, one group of cells (SE-cells, n = 207) was strongly excited during saccadic eye movements, but they were considerably less active at intermissions of the eye movements. In contrast, the other group of cells (SD-cells, n = 55) was active when the eyes remained stationary, and was depressed during the eye movements. Almost all of the striate cells (271/284) studied exhibited a change in their activity in conjunction with eye movements, so they could be classified into these two groups except for a very few cells (9/271) which exhibited an intermediate response (initial excitation and later depression). Saccade-excitation in the SE-cells frequently contained two components, i.e. an initial component occurring after the onset of eye movements (latency, about 20 ms) and a later component following the initial component with a delay of about 50 ms. The initial component occurred in the presence of a visual pattern and disappeared in darkness, suggesting that it represents a type of the retinal reafference signaling movement of the retinal image caused by the eye movement36. The later component was extra-retinal in origin, since it persisted in darkness 36. Therefore, the SE-cells seem to receive two types (retinal and extra-retinal) of signals of eye movement. These findings are in partial agreement with previous studies 26'27"3s reporting extra-retinal excitation in a relatively small number of striate cells. The cause of this discrepancy in the percentage of cells receiving extra-retinal s accade-excitation (10 % in Noda et al?6, 24 in Vanni-Mercier and Magnin 38, and 75% (126/167) in the present study) is unclear, but may be attributed to different experimental conditions. In the previous studies 26'3s the animal was simply kept in darkness, while in the present study it was strongly motivated to make saccadic eye movements with rewards. It was found that extraretinal excitation was frequently reduced, and even disappeared, in the present study when the animal received sufficient rewards and became drowsy so that eye movements became slow. Therefore, extra-retinal excitation may occur only when the animal is fully alert and makes quick eye movements. Correspondence between saccade-related activity and photic responsiveness Under suppression of eye movements by withdrawal of rewards or retrobulbar block, almost all SD-cells (23/26) exhibited the photic responsiveness reported for the "simple" cells in the anesthetized cat, and most of the SE-cells (89/104) that for the

220 "complex" cells. Therefore, it is likely that the SD- and SE-cells classified on the basis of their eye movement-related activity correspond to the "simple" and "complex" cells. These two major neuronal populations in the striate cortex may provide parallel channels for visual information that are gated in an alternate way by signal of eye movements, the former channel being closed while the latter channel is open during the period of eye movements. This view is consistent with the contrasting modulatory effects of passive movement of a textured visual stimulus on the "simple" and "complex" cells J0. In the present study, the number of "simple" cells was about one-third that of the "complex" cells, which is significantly smaller than those reported in previous studies 7,1235,19,33. The relatively large percentage of"complex" cells in the total population of the striate cells is probably ascribable to the relatively coarse metal electrodes used for sampling the cells, penetrating through the dura which overlies the striate cortex. A coarse rnicroelectrode may favor sampling of the "complex" cells, with a larger soma than the "simple" cells. Neural basis for eye movement-related activity in SE- and SD-cells It is pointed out that the SE- and SD-cells of the striate cortex behaved in much the same way as the y- and the x-geniculate cells of the alert cat, respectively23"24. Both the SE-cells and y-geniculate cells were active during eye movement and less active at intermissions, and vice versa the SD-cells and x-geniculate cells. The latencies of depression in the x-cells and excitation in the y-cells (both about 30 ms) roughly agree with those of saccade-excitation in the SE-cells (20 ms, el. Table I and also Fig. 3A and B) and saccade-depression in the SD-cells (30 ms, cf. Table I and Fig. 5A and B). Excitation in the y-cells and depression in the x-cells both disappear in darkness. Therefore, it is likely that the retinal component of saccade-excitation in the SE-cells is caused by excitatory inputs from the y-geniculate cells, while saccade-depression in the SD-cells is caused by disfacilitation due to removal of tonic inputs from the x-geniculate cells 22-25'3°,36. The stronger activity in the SD-cells than the SE-cells at intermissions of eye movement may also be explained by the above scheme. The tonic activity in the SD-cells probably reflects the excitatory inputs from the x-geniculate ceils that are much more sensitive than the y-cells to small drifts of eye position occurring at intermissions of eye movement23'24. It is notable that the tonic activity in the SD-cells disappeared under retrobulbar paralysis of eye movement. Therefore the activity may be maintained by active rather than passive drifts that are abolished by paralysis of eye movement. The neural mechanisms for the extra-retinal excitation are unclear at present, and will be a subject of a future study. In summary, the present investigation demonstrates that integration of the retinal and extra-retinal signals of eye movement is performed at least partly in the visual cortex. The integration is not simple subtraction of the motor signals of eye movements from reafferent retinal signals as was supposed by the cancellation hypothesis 11,32. The

221 visuo-motor integration is performed in a more complicated way through the visual channels corresponding to the "simple" and "complex" cells. The former channel may be closed by the retinal reafference2°'=~'36 and the latter channel may be opened by both retinal and extra-retinal signals of eye movements 36. Suppression of the "simple" channel might be a neuronal correlate of saccadic suppression ~8'39 while activation of the "complex" channel might represent visual evaluation of eye movement21. ACKNOWLEDGEMENTS

We wish to thank Professor M. Ito for constant encouragement during the work. This work was supported by Grant-in-Aid for Scientific Research Project (57440027) and Grant-in-Aid for Special Project Research (410808) from the Japanese Ministry of Education, Science and Culture, and a Grant of the Mitsubishi Foundation.

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