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The relationship between response characteristics to flicker stimulation and receptive field organization in the cat's optic nerve fibers
Vision
RN. Vol. 11, pp. 227-240. Persamon Prcu 1971. Printed in Great Britain.
THE RELATIONSHIP BETWEEN RESPONSE CHARACTERISTICS TO FLICKER STIMULATION AND RECEPTIVE FIELD ORGANIZATION IN THE CAT’S OPTIC NERVE FIBERS YOSHJRO FUKADA Research Group on Auditory
and HIDE-AKI SAITO
and Visual Information Processing, NHK Broadcasting Laboratories, Setagaya-ku, Tokyo, Japan
Science Research
(Received 9 April 1970; in t-eked form 10 July 1970)
INTRODUCTION THE RECEPTIVE fields
most commonly found in the cat’s retinal ganglion cells are composed of an excitatory or inhibitory center and an antagonistic surround. In the preceding paper (FUKADA,1971), these receptive fields have been classified into two types : Type I and Type II, according to ditferences in the time course of the response to a stationary light spot in the center of the receptive field. A Type I-cell responds briskly to an abrupt change in the luminance of the spot, but it does not continue to discharge to a stationary light spot. This is in contrast to a Type II-cell, which continues to discharge to a stationary light spot. From the above facts, it is to be expected that the two types of ganglion cells would exhibit distinctly different behavior to intermittent photic stimulation. In the previous experiment on individual fibers of the cat optic nerve, a positive correlation was found between conduction velocity and the highest flicker frequency which the individual fibers followed in a one-to-one correspondence between gash and response (CCF) (FUKADA,MOTOKAWA,NORTONand TASAKI, 1966). The primary purpose of the present study is to examine how the responsiveness to flicker stimulation is related to the receptive field type. In addition, observations were made on the relationship between the responsiveness to flicker stimulation by light spot placed at the center of the receptive field and the conduction velocity of optic nerve fibers. METHODS Experiments were performed on adult cats. They were anaesthetixed with Nembutal and immobilized by gallamine triethiodide. Surgical procedures, recording methods, measurements of conduction velocity and mapping of receptive fields have been fully described in a preceding paper (FLJKADA,1971). Recordings were made with either tungsten microelectrodes or 3M-KCI-filled glass micropipettes stereotaxically placed in the region of the optic chiasm. Stimulating electrodes were inserted into the optic tract near its entrance to the lateral geniculate body. The conductionvelocityof single fibers was determined dividing the distance between the stimulating and recording sites by the latency of the antidromic spike. The photic stimulus was a spot of light subtending l/4” at the cat’s eyes, and produced by a glow modulator tube (Sylvania R1131C): the luminance was modulated 80 per cent at l-100 Hz in a square wave fashion (average luminance, 1.08 x lo3 cd/m2). The luminanceof the background was 1.5 cd/m*. Gccasionally, the spot luminance was modulated in a sine wave fashion. t A part of this work was presented at the Japan-U.S. Joint Seminar on Nervous Mechanisms of Vision and Visual Behavior held in Kyoto, Japan on 4-8 November 1969. 227
228
YOSHIRO Furm~.um
HIDE-/&IS-
RESULTS
single fiber response was isolated by a microelectrode. First, on of the to diffuse to a stationary spot, it was I or of four in response to flickering in Fig. 1. At a low flicker frequency, the temporal spacing of the grouped spikes corresponds to the interval between cycles of flicker. Thus the spike discharge pattern may be said to follow the flicker frequency. In the previous study (FUKADA et al., 1966), two distinct points of transition in spike discharge have been defined along the llicker frequency continuum: CCF and CFF. ON-II
OFF-I
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_-_--_----_______-___-_ 20
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FIG. 1. Discharge patterns of each record is stimulus mark; size in column On-I is 6 mV; figures were played back on
On-I, Off-I and On-II upward displacement Off-I, 5 mV; On-II, an oscilloscope screen
fibers to flicker stimulation. Top trace in indicates the increase in luminance. Spike 2.5 mV. Records in this and subsequent from magnetic tape and photographed.
The CCF (critical correspom&ngjieqwncy) has been defmed as the highest flickar frequency at whkh the response f&Iowa or corresponds faithfnliy to individual flashes, At siiSbtly h&ber Gieker frequenci~ the spike discbarge pattern. a~~o~~ it fails to follow the Bicker frequency, is quite different from the response to steady fight. At still bigber Bicker fqneney, the response to Bicker becomes indistinguishable from the response to steady light. This latter frequency has been deBned as the CFF (critical j&km frequency, or critical fusion fieguency), which may be conformable to the psychophysical definition. Since the CFF bad been fonnd to be closely reh&d to the CCF and the Wsr was easier to determine, the CCF was adopted as the index of Bicker ~~~~vit~ in eachunit in the present e~~rirne~~ i.e. the CCF was judged to have heen reached when the cell failed to follow 20 conseontive Sashes. Relation ofcondircriontielocityto CCF Both CX!F and conduction veioeity were measured in 185 fibers: On& 4gs;Of&I, 85; On-fF, 50; O&U, 0Ilry one; the remaming one was nn&ss%ed. In Fig. 2 the CCF is plotted against the ~o~du~~on veXoeity(A, ‘On’“-oenter; B, %B’” center). For Type I-fibers which are represented by black rectangles in Fig. 2, there is a
Fm. 2. Cme~ational diagram between CCF and conduction velocity. Ordinate: CCF. Abscissa: conduction velocity. A, “On”-center fibers. B, “W-cater fibem. Filledreciunglero mpmcnt Type I; open recmgk~, ‘&pe Ii; recmgk8 w&h Q cross, “Unclwified”. The am of each recta@e iti proportionai to nuinber of fibers eammred.
though very weak degree of correlation between the CCF and the conduction correlation ratio of CCF on velocity (E,,) for On-1 fibers is O-47,while for Off-I fibers jrs,, is 060. Type II-fibers offered astrikingcontrast toType I-fibers. Asshown in Fig, 2A fonaa), the CCF for Un-if fibers did nut show any tendency to vary with condnetion velocity.
psi&e, velocity.
Tim
One of the distinctive fe&tures of On-II fibers, which can be seen in Fig. 2, is that the distribution of the CCF is divided into two parts, one very low (‘fessthan ten) and the other
230
Yosmao FUKADAAND HIDE-AKI S.UTO
very high. This fact suggests that On-II fibers are composed of two different groups with respect to responsiveness to flicker stimulation. There was no remarkable difference among On-II fibers in the manner in which they responded to diffuse light and to restricted light modulated in luminance at very low frequency. The On-II fibers which showed a low CCF, however, had a tendency to be more labile in their responsiveness than those which showed a high CCF. Closer inspection revealed that On-II fibers with low CCF often stopped their firing for several hundred msec. One example of On-II with a low CCF is shown in Fig. 3A. This unit
A ON-It ON-n:
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FIG. 3. A, Discharge patterns of On-II-L to flicker stimulation. Spike size is 3 mV. Stimulus marks same as Fig. 1. B, Comparisons between On-II-L and On-II-H. Upper histogram: Frequency distribution of position of On-II cells in the retina. Abscissa: distance from area cenlrulis. Black 6urs represent On-II-L; hirebars, On-II-H. Lower histogram: Frequency distribution of size. Abscissa: size of receptive field center. BIuclc bars represent On-IIL; white bars, On-II-H.
responded faithfully to flicker up to 4 Hz. At higher flicker frequency it sometimes stopped firing for several hundred msec, but while firing it would follow flicker frequencies up to nearly 40 Hz. In some On-II cells background impulse discharges prevailed over the responses to flicker, resulting in a very low CCF. For the present, we shall distinguish between On-II units which showed a very low CCF (On-II-L) and other On-11 units (On-IIH). On-II-L cells have been found to have a tendency to be located more centrally in the retina than On-II-H, as shown in Fig. 3B (upper histogram). All the On-II-L cells were located in the area less than 20” from the central part of the retina. This difference of
231
Responseto Flicker in Cat Optic Nerve
distribution of the two types of On-II units is statistically significant at the 0405 level. Fig. 3B (lower histogram) shows that the diameter of the receptive field center of On-II-L is smaller than that of On-II-H (p ~0405). Average impulse frequency during flicker stimulation Many investigators have reported that the average impulse frequency of retinal ganglion cells in response to diffuse flicker stimulation first increases as the flicker frequency increases, reaches a maximum, and then decreases (GR~~SSER and CIUXJTZFELDT, 1957; GROSSERand BABELO,1958; FUKADA et al., 1966; HUGHES and MAFFEI,1966). Similar behavior to a spot stimulus has also been noted (CLELANDand ENROTH-CUGELL,1966 ; B~ITNEX and GRWER, 1968). Some examples of average impulse frequency during flicker stimulation are shown in Fig. 4. OFF-I
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FIG. 4. Relation between average impulse frequency and &cker frequency for several cells in each of four categories. Arrow on each curve indicates the point at which response pattern fails to follow flicker frequency (CCF). Oblique &shed lines pass the points such that the average impulse frequency is equal to the ticker frequency.
For On-II units, the average impulse frequency did not change remarkably with the ticker frequency. This is one of the most distinct features of On-II cells. For Type I-cells (On-I and Off-I), on the other hand, the impulse frequency increased to a maximum and then decreased as the flicker frequency was farther increased: at the CCF the impulse frequency was nearly equal to the flicker frequency. Some Type I-cells showed curious behavior: when stimulated repeatedly by flicker at an appropriate frequency near which the maximum impulse frequency occurred, these cells began to discharge periodically at about 200
A
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ptrttcm of 811Uff-I to Bicker st~mulatjou. B, Time course of indwsd %. 5. A, Dhh’g~ fbztkity of the same ccl1by about 14 HZ flicker, C, InduCea activity; at urrow 1, Bicker stimu_ lationtakcn away; at 6zrruw2, flicker stimulation given again. Spike site; 3 mV.
Response to Flicker in Cat Optic Nerve
233
impulses/set, superimposing this pattern upon the response to individual flashes of flicker. This induced impulse discharge will be described in more detail later. The response characteristics of the two types may be summarized as follows: the average impulse frequency of Type I varies as a function of flicker frequency, but that of Type II is independent of flicker frequency. Repetitive firing induced by flicker The average impulse frequency in Type I-cells was dependent on flicker frequency, as described above. When the flicker frequency was continuously and gradually changed around that frequency which elicited the maximum impulse average, some Type I-cells, which had a receptive field with a distinctive surround, showed impulses in addition to those bursts of impulses which corresponded to the individual flashes of flicker. When the flicker frequency was adjusted properly, these additional impulses increased and occurred midway in the interval between those bursts of impulses evoked by the individual flashes of flicker. We shall call this phenomenon induced activity. One example of induced activity in a Off-I unit is shown in Fig. 5. Figure 5A shows the impulse discharge patterns to flicker when the frequency of flicker was changed stepwise. Impulse discharges followed faithfully the flicker frequency up to 35 Hz, but when this unit was repeatedly stimulated by flicker at 14.1 Hz for about 10 set, induced firing occurred as shown in Fig. 5B. Induced activity was usually found to continue for as long as several tens of seconds and to be composed of regularly spaced impulses at about 200 Hz. These impulses were not time locked to the stimulus. During the induced activity, this cell continued to respond to individual flashes of flicker, overlapping the regularly spaced discharges. In the last stage of induced activity, impulses often fell out. This activity could be induced again by fmely re-tuning the flicker frequency. When 5icker stimulation was removed in the course of induced activity (Fig. 5C, arrow l), only the regularly spaced impulses remained, but the direct photic responses reappeared when flicker stimulation was recommenced (Fig. 5C, orrow 2). In Fig. 6, another example of induced activity is shown. In this On-I cell, induced activity was occurred when a flicker frequency was maintained at 30 Hz for longer than 10 sec. Induced activity, once it occurred, was not affected by a change of flicker frequency (Fig. 6B); it lasted for about 40 set after its initiation. The flicker frequency at which induced activity occurred, varied with the individual cell between about 10 and 30 Hz. Some cells showed induced activity only under the dark background condition. As is shown in Fig. 7A, an Off-I cell increased its impulse frequency to as high as 100 impulses/set at 20 Hz flicker under the light background condition, but it did not show induced activity. When the background light was removed, the maximum impulse frequency increased rapidly with flicker frequency and showed induced activity at 9.9 Hz flicker. Another Off-I cell showed induced activity under a variety of stimulus conditions (Fig. 7B). The flicker frequency at which induced activity occurred, was about the same (13*5-14.5 Hz) in every case. This cell showed some instability of the discharge pattern at low flicker frequencies under the condition of dark background and weaker stimulus intensity. It was occasionally observed that shadows which passed rapidly over the receptive field or that flicking the room light on and off initiated the induced activity when the tuned flicker frequency was not yet enough to induce the activity. Other kinds of periodic discharge patterns were also observed in the cells which did not
YOSHIROFUKADA AND HIDE-AKI SAITO
234
set
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203 m set FIG. 6. A, Discharge patterns of an On-I to flicker stimulation. B, Induced activity of the same cell. It was induced by 30 Hz flicker, then flicker frequency was shifted to 20 Hz, 10 Hz
and 1 Hz, successively. Spike size; 2 mV. have such a strong surround as those which showed the induced activity. In Fig. 8A spontaneous periodic activity in the light adapted state is shown. Another exampie of periodic@ in maintained activity of an Off-I cell is shown in Fig. 8B. When the room light was turned off (Fig. 8B, arrow), the maintained discharge rate increased and some periodicity was observed {marked by a broken line on the right side of the records). Periodic firing in the maintained activity, similar to that described above, was not observed in the cell which exhibited induced activity.
Response to Flicker in Cat Optic Nerve
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g s 150a L
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FIG.7. Relation between average impulse frequency and flicker frequency for two Off-I cells which showed the induced activity. Stimulus condition as indicated. Other characteristics of the response to flicker
The CCF/intensity relation was also studied. The peak luminance of the light spot during the flicker was usually 1.94 x IO3 cd/m2. For some cells spot luminance was reduced with neutral density filters. Both Type I and Type II showed a definite tendency to lower the CCF as stimulus intensity was decreased (Fig. 9). This behavior was generally the same as that previously found with diffuse light stimuli in either dark or light adapted eyes (ENROTH, 1952; DODT and ENROTH, 1954; FUKADA et al., 1966) and with larger light spots (OGAWA et al., 1966). There has so far been no demonstrable difference between Type I and Type II -cells. The relation between CCF and maximum impulse frequency during flicker stimulation was studied next. With diffuse light stimuli, it had been previously shown (FUKADA et al., 1966) that all cells exhibited the same curvilinear functional relation expressed generally as: CCF = L [l-exp(-u.ZF,,,)] where ZF,,, = maximum impulse frequency (impulses/set) L = the upper limit of the CCF for a given set of stimulus conditions a = aconstant. In the present experiment, the CCF was plotted against the maximum impulse frequency as shown in Fig. 10. In all Type I-cells (circles and squares) there was a definite relation between CCF and maximum impulse frequency. A curve fitted to the observed points for Type I-cells, including those which showed induced activity, is shown in Fig. 10 by the broken line. This curve can be expressed as: CCF = 52 [l -exp(-0~0144ZF,,,,,)].
(1)
236
-
!OOmsec
This equation is of the same form as that obtained with diffuse light. It may als0 be noted that the #‘_ of Type I-ceils which have shown the induced activiQ a and El in Fig. 10) is tigber than the IF,, of tie otier Type I-cells (@ and 0) ; all of &em show more than 120 impuls~~sec. Type &cells (+ + -!-+) present a strong cantrast with Type I. They are divided into two groups and fall far away from the curve expressed by equatian (1). Therefore it is conceivable
Response to Flicker in Cat Optic Nerve
231
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Log LIGHT INTENSITY FIG. 9. CCF as a function of light intensity. Abscii:
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FIO. 10. Relation between CCF and maximum impulse frequency for each type of cell. RepresentOn-I;(Wn H W)On-1 which showed induced activity; (0 0 0 0) O&I; (OOClO) Off-I which showed induced activity; (+ +++) On-II. Broken curve is drawn from equation 1 (see text). (~~~>
that the response characteristics of Type I and Type II to flicker stimulation are distinctly different. DISCUSSION The difference between Type I- and Type II-cells in response to flicker stimulation has been confirmed in this experiment. As the flicker frequency increases, the average impulse frequency in Type I-cells increases, passes through a maximum, and finally falls off. On the
other hand, the average impulse frequency in Type II-cells remains almost unchanged over a wide range of fficker frequencies, though many Type IE-cells can foilow even higher flicker frequencies than Type f-ceils. It is possible that Type If-cells may respond with the same average impufse frequency to a spot of tight if csn%ythe average fuminance is unchanged, Some Type II-cells exhibited labile responsiveness to flicker stimulation. These celis are not qualified to transfer temporal information, but they are competent for processing spatial information because their receptive field is small, centrally located and is most sensitive to stationary small objects. Type I-cells, in contrast with Type IX, are suitable far processing tem~o~l info~matio~~ as they ~~~~~t~~t~ the light stimulus with respect to time_ Concerning the relationship between CCF and conduction velocity, it is probable that almost all of the fibers which have been studied in the previous paper (FURADA et al., 1966) are Type I-cells, because under the condition of diffuse illumination Type II-cells respond oniy weakIy to flicker. The relation between CCF and conduction velocity obtained with a spot stimulus, was not as clear as that obtained with diffuse Iight. One of the probable reasons for this d%erence is that spatial summation over the whole receptive geld of a Type f-cell results in a smoothing out of the regional variations in responsiveness to flicker, MAFFEI (1968) has shown that the spatial average at the lateral geniculate body can achieve a smoothing and improve the signal-to-noise ratio in sine-wave responses. If the presence of this averaging effect is demonstrated in Type f-cells in the retina, it becomes more probable that the Type I-cell is suitable for deteoting a temporal change in the average intensity of light rather than the spatial difference in light intensity in its receptive Geld, Concerning the periodic activity in the visual system, a number of investigators have noted that periodic activities can be evoked by light flashes or affected by conditions of illumination (Dam and KKMURA,1963; CRAPPER and NQELL, 1963; BROWNand ROJAS, 1965; OGAWA, Bmo~ T_.mmz and ~~EAN~~
and L~vrcrc, 1966;
STEPGERG, 1966; STONEand FABXAN, 1966;
1967; PACRECO, BEAR arrd ERWN,
1968). Periodicity is also observed discharges (HEM and BORNXHE~, 1966; ~Efss, I%?; %XMXDT and CREUTZFELDT, 1968). It has been reported that there is an increased tendency to repetitive firing under barbiturate anaesthesia (KUFFLER,FITZHUGH and BARLOW,1957; DOTY and KIMURA,1963; BROWNand RCHAS,1965). In the present study cats were anaesthetized with Nembutal, Both the periodic bursts of spontaneous discharges in light (Fig. 8A) and the periodic@ observed when the room light was turned off (Fig, SB& seem r&ted to those phenomena already reported in the literature. However, in several respects, the induced activity is different from those phenomena previously reparted. The frequency of induced firing is very high (about 200 Hz), and it continues for as long as one minute with highly regular spike intervals. Once it has begun neither a change of flicker frequency nor withdrawal of the light stimulus has any elect on stopping the induced activity. Ganglion cells do not either change their ~s~ns~~enes~ to pbotic stimulation during the induced activity or show any sign of depression such as seen in the case of the retinal spreading depression (GOURAS,19%). Fifteen Type I-cells (On-I, 8; Off-I, 7) out of 32 Type I-cells which have exhibited a distinct surround response, have shown the induced activity. These are all cells which have reached a maximum impulse frequency of more than 120 impulses/see. Although a s~tem~t~c ~xarn~~at~o~ on the effect of drugs has not been attempted, an ad~t~on~ dose of Nembutaf (about fO m&kg) seemed to have no e&ct on induced activity. The above observations suggest to us that the induced activity may have some connection with the neuronal organization of the receptive field. The occurrence of the repetitive discharges of constant frequency in addition to transient bursts which follow in spontaneous
Response. to Flicker in Cat Optic Nerve
239
flickering light, may suggest that the ganglion cells receive long-lasting depolarizing inputs by a means different from the main path which conveys the flicker information through the retina, but no direct evidence of this interpretation has yet been obtained.
SUMMARY (1) The average impulse frequency in Type I-fibers (phasic type) increases, passes through a maximum, and finally falls off, as the flicker frequency increases. On the other hand, the average impulse frequency in Type II-fibers (tonic type) remains almost unchanged over a wide range of flicker frequencies. (2) In Type I, the highest flicker frequency at which the unit responds faithfully to individual fiashes (CCF), is correlated positively with conduction velocity. For Type II the CCF is not correlated with conduction velocity. Some Type II-units change responsiveness during flicker stimulation, and often stop the firing for several hundred msec. (3) In all Type I-fibers there is a definite relation between the CCF and the maximum impulse frequency, while in Type II the relation between them is not clear. (4) The majority of Type I-fibers which had a distinct antagonistic surround in their receptive field showed repetitive firing at high frequency (about 200 Hz) when the flicker frequency was adjusted properly around the frequency which elicited the maximum impulse frequency. (5) It is concluded that Type I is suitable for processing temporal information, while Type II is suitable_ for processing spatial information. Acknowledgnrenrs-The authors would like to thank Prof. K. TASAKI for his encouragement and for valuable suggestions on the manuscript. They are very grateful to Drs. A. C. NORTONand J. I. SIMPXINfor a critical reading of the manuscript.
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butal). PfGgers Arch. ges. Physiol. 300, 129-147. STB~BERG, R. H. (1966). Oscillatory
activity in the optic tract of cat and light adaptation. J. Neurophysiol. 29, 139-l 56. STONE, J. and FABUN, M. (1966). Specialized receptive fields of the cat’s retina. Science, N. Y. 152, 12771279.
Abstract-The response characteristics of cat’s optic nerve fibers to flicker stimulation were investigated. As the flicker frequency increases, the average impulse frequency in Type Ifibers (phasic type) increases, passes through a maximum, and finally falls off. When the flicker frequency is adjusted properly, Type I-fiber which has a distinct surround in its receptive field shows a repetitive firing at high frequency (about 200 Hz). The average impulse frequency in Type II-fibers (tonic type) remains almost unchanged over a wide range- of flicker frequencies. R&urn&On &udie les caracteristiques de la reponse des fibres du nerf optique du chat a une stimulation papillotante. Quand la frtquence du papillotement augmente, la frequence moyenne des imp&ions des fibres du Type I (type phasique) augmente, passe par un maximum, et finalement diminue. Quand la frequence du papillotement est convenablement choisie, la fibre du Type I qui posdde un bord distinct dam son champ rkcepteur posskde une rkponse rbpktitive A grande fr&uence (vers 200 Hz). La frkquence moyenne d’impulsions des fibres du Type II (type tonique) reste presque sans changement dans un grand domaine defrequences de papillotement. Zusammenfassung-Es wurden die Antwortskennzeichen der Katzenoptikusfasern fiir Flimmerreize untersucht. Wenn sich die Flimmerfrequenz erhiiht, so steigt die mittlere Antwortsfrequenz der Fasem des Typus No. I (des phasischen Typus), erreicht einen Gipfel und vermindert sich am Ende. Wenn die Flimmerfrequenz richtig justiert ist. so zeigt Typus No. 1, welcher ein klares Umfeld in seinem Rezeptivfeld besitzt, eine wiederholte Hochfrequenzentladung (cu. 200 Hz). Die Mittelentladungsfrequenz der Fasem des Typus No. 2 (des ton&hen Typus) bleibt bei einem grossen Flimmerfrequenzbereich beinahe unverandert. aono~oH 3prftwrbHoro HepBa ~ounof B c~~~fyHauruo (hfe~5ruuotu~ii CB~T). Korga YBcTora ~e.nbzamiii ywcs, cpextuur 9acrora ribfnynbco~ BO~OKOHI-r0 mna (@ta~secrrnB rsm) riapacmer, npoXonnT Yew3 MaYCuMyM H, B KOHlre KOHUOB,naJB%T. EUIH YBcIy)Ta MeJtBKaHHHpel-yHB* pyeTUl TOYHO.TO BOlIOKHaI-r0 THlTa,KOTOpbteHMelOTB HX peuetTTHB.iiOMnone OnpeHeJteHHOe ~HB~aHBHoe OKp)meBHe, O6HapyZKHB;uoT nOBTOpBbIe pa3pKJ&t BbrcoKOti YacTOTbl (OKoHo 200 l%pn). GpeAHiul YiiCTOTZ3 HMITynBcoB BOnOKOHII-r0 TAna (TOHHYeCK& T%Hl) ocT8eTcII noYTB HeH3MeBHOftB npeAenaX IIIEpOKOrO JWaIW3OHB YXTOTbI MIXbKBiEii.
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RN. Vol. 11, pp. 227-240. Persamon Prcu 1971. Printed in Great Britain.
THE RELATIONSHIP BETWEEN RESPONSE CHARACTERISTICS TO FLICKER STIMULATION AND RECEPTIVE FIELD ORGANIZATION IN THE CAT’S OPTIC NERVE FIBERS YOSHJRO FUKADA Research Group on Auditory
and HIDE-AKI SAITO
and Visual Information Processing, NHK Broadcasting Laboratories, Setagaya-ku, Tokyo, Japan
Science Research
(Received 9 April 1970; in t-eked form 10 July 1970)
INTRODUCTION THE RECEPTIVE fields
most commonly found in the cat’s retinal ganglion cells are composed of an excitatory or inhibitory center and an antagonistic surround. In the preceding paper (FUKADA,1971), these receptive fields have been classified into two types : Type I and Type II, according to ditferences in the time course of the response to a stationary light spot in the center of the receptive field. A Type I-cell responds briskly to an abrupt change in the luminance of the spot, but it does not continue to discharge to a stationary light spot. This is in contrast to a Type II-cell, which continues to discharge to a stationary light spot. From the above facts, it is to be expected that the two types of ganglion cells would exhibit distinctly different behavior to intermittent photic stimulation. In the previous experiment on individual fibers of the cat optic nerve, a positive correlation was found between conduction velocity and the highest flicker frequency which the individual fibers followed in a one-to-one correspondence between gash and response (CCF) (FUKADA,MOTOKAWA,NORTONand TASAKI, 1966). The primary purpose of the present study is to examine how the responsiveness to flicker stimulation is related to the receptive field type. In addition, observations were made on the relationship between the responsiveness to flicker stimulation by light spot placed at the center of the receptive field and the conduction velocity of optic nerve fibers. METHODS Experiments were performed on adult cats. They were anaesthetixed with Nembutal and immobilized by gallamine triethiodide. Surgical procedures, recording methods, measurements of conduction velocity and mapping of receptive fields have been fully described in a preceding paper (FLJKADA,1971). Recordings were made with either tungsten microelectrodes or 3M-KCI-filled glass micropipettes stereotaxically placed in the region of the optic chiasm. Stimulating electrodes were inserted into the optic tract near its entrance to the lateral geniculate body. The conductionvelocityof single fibers was determined dividing the distance between the stimulating and recording sites by the latency of the antidromic spike. The photic stimulus was a spot of light subtending l/4” at the cat’s eyes, and produced by a glow modulator tube (Sylvania R1131C): the luminance was modulated 80 per cent at l-100 Hz in a square wave fashion (average luminance, 1.08 x lo3 cd/m2). The luminanceof the background was 1.5 cd/m*. Gccasionally, the spot luminance was modulated in a sine wave fashion. t A part of this work was presented at the Japan-U.S. Joint Seminar on Nervous Mechanisms of Vision and Visual Behavior held in Kyoto, Japan on 4-8 November 1969. 227
228
YOSHIRO Furm~.um
HIDE-/&IS-
RESULTS
single fiber response was isolated by a microelectrode. First, on of the to diffuse to a stationary spot, it was I or of four in response to flickering in Fig. 1. At a low flicker frequency, the temporal spacing of the grouped spikes corresponds to the interval between cycles of flicker. Thus the spike discharge pattern may be said to follow the flicker frequency. In the previous study (FUKADA et al., 1966), two distinct points of transition in spike discharge have been defined along the llicker frequency continuum: CCF and CFF. ON-II
OFF-I
ON-I
Hz.
2
5
IO
_-_--_----_______-___-_ 20
30
________________________ _____________________--__ 40
50
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.......
.._..“..._
...............
..^
.._ _.--._.-
_
--
A
100 -
FIG. 1. Discharge patterns of each record is stimulus mark; size in column On-I is 6 mV; figures were played back on
On-I, Off-I and On-II upward displacement Off-I, 5 mV; On-II, an oscilloscope screen
fibers to flicker stimulation. Top trace in indicates the increase in luminance. Spike 2.5 mV. Records in this and subsequent from magnetic tape and photographed.
The CCF (critical correspom&ngjieqwncy) has been defmed as the highest flickar frequency at whkh the response f&Iowa or corresponds faithfnliy to individual flashes, At siiSbtly h&ber Gieker frequenci~ the spike discbarge pattern. a~~o~~ it fails to follow the Bicker frequency, is quite different from the response to steady fight. At still bigber Bicker fqneney, the response to Bicker becomes indistinguishable from the response to steady light. This latter frequency has been deBned as the CFF (critical j&km frequency, or critical fusion fieguency), which may be conformable to the psychophysical definition. Since the CFF bad been fonnd to be closely reh&d to the CCF and the Wsr was easier to determine, the CCF was adopted as the index of Bicker ~~~~vit~ in eachunit in the present e~~rirne~~ i.e. the CCF was judged to have heen reached when the cell failed to follow 20 conseontive Sashes. Relation ofcondircriontielocityto CCF Both CX!F and conduction veioeity were measured in 185 fibers: On& 4gs;Of&I, 85; On-fF, 50; O&U, 0Ilry one; the remaming one was nn&ss%ed. In Fig. 2 the CCF is plotted against the ~o~du~~on veXoeity(A, ‘On’“-oenter; B, %B’” center). For Type I-fibers which are represented by black rectangles in Fig. 2, there is a
Fm. 2. Cme~ational diagram between CCF and conduction velocity. Ordinate: CCF. Abscissa: conduction velocity. A, “On”-center fibers. B, “W-cater fibem. Filledreciunglero mpmcnt Type I; open recmgk~, ‘&pe Ii; recmgk8 w&h Q cross, “Unclwified”. The am of each recta@e iti proportionai to nuinber of fibers eammred.
though very weak degree of correlation between the CCF and the conduction correlation ratio of CCF on velocity (E,,) for On-1 fibers is O-47,while for Off-I fibers jrs,, is 060. Type II-fibers offered astrikingcontrast toType I-fibers. Asshown in Fig, 2A fonaa), the CCF for Un-if fibers did nut show any tendency to vary with condnetion velocity.
psi&e, velocity.
Tim
One of the distinctive fe&tures of On-II fibers, which can be seen in Fig. 2, is that the distribution of the CCF is divided into two parts, one very low (‘fessthan ten) and the other
230
Yosmao FUKADAAND HIDE-AKI S.UTO
very high. This fact suggests that On-II fibers are composed of two different groups with respect to responsiveness to flicker stimulation. There was no remarkable difference among On-II fibers in the manner in which they responded to diffuse light and to restricted light modulated in luminance at very low frequency. The On-II fibers which showed a low CCF, however, had a tendency to be more labile in their responsiveness than those which showed a high CCF. Closer inspection revealed that On-II fibers with low CCF often stopped their firing for several hundred msec. One example of On-II with a low CCF is shown in Fig. 3A. This unit
A ON-It ON-n:
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FIG. 3. A, Discharge patterns of On-II-L to flicker stimulation. Spike size is 3 mV. Stimulus marks same as Fig. 1. B, Comparisons between On-II-L and On-II-H. Upper histogram: Frequency distribution of position of On-II cells in the retina. Abscissa: distance from area cenlrulis. Black 6urs represent On-II-L; hirebars, On-II-H. Lower histogram: Frequency distribution of size. Abscissa: size of receptive field center. BIuclc bars represent On-IIL; white bars, On-II-H.
responded faithfully to flicker up to 4 Hz. At higher flicker frequency it sometimes stopped firing for several hundred msec, but while firing it would follow flicker frequencies up to nearly 40 Hz. In some On-II cells background impulse discharges prevailed over the responses to flicker, resulting in a very low CCF. For the present, we shall distinguish between On-II units which showed a very low CCF (On-II-L) and other On-11 units (On-IIH). On-II-L cells have been found to have a tendency to be located more centrally in the retina than On-II-H, as shown in Fig. 3B (upper histogram). All the On-II-L cells were located in the area less than 20” from the central part of the retina. This difference of
231
Responseto Flicker in Cat Optic Nerve
distribution of the two types of On-II units is statistically significant at the 0405 level. Fig. 3B (lower histogram) shows that the diameter of the receptive field center of On-II-L is smaller than that of On-II-H (p ~0405). Average impulse frequency during flicker stimulation Many investigators have reported that the average impulse frequency of retinal ganglion cells in response to diffuse flicker stimulation first increases as the flicker frequency increases, reaches a maximum, and then decreases (GR~~SSER and CIUXJTZFELDT, 1957; GROSSERand BABELO,1958; FUKADA et al., 1966; HUGHES and MAFFEI,1966). Similar behavior to a spot stimulus has also been noted (CLELANDand ENROTH-CUGELL,1966 ; B~ITNEX and GRWER, 1968). Some examples of average impulse frequency during flicker stimulation are shown in Fig. 4. OFF-I
10
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30
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FIG. 4. Relation between average impulse frequency and &cker frequency for several cells in each of four categories. Arrow on each curve indicates the point at which response pattern fails to follow flicker frequency (CCF). Oblique &shed lines pass the points such that the average impulse frequency is equal to the ticker frequency.
For On-II units, the average impulse frequency did not change remarkably with the ticker frequency. This is one of the most distinct features of On-II cells. For Type I-cells (On-I and Off-I), on the other hand, the impulse frequency increased to a maximum and then decreased as the flicker frequency was farther increased: at the CCF the impulse frequency was nearly equal to the flicker frequency. Some Type I-cells showed curious behavior: when stimulated repeatedly by flicker at an appropriate frequency near which the maximum impulse frequency occurred, these cells began to discharge periodically at about 200
A
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ptrttcm of 811Uff-I to Bicker st~mulatjou. B, Time course of indwsd %. 5. A, Dhh’g~ fbztkity of the same ccl1by about 14 HZ flicker, C, InduCea activity; at urrow 1, Bicker stimu_ lationtakcn away; at 6zrruw2, flicker stimulation given again. Spike site; 3 mV.
Response to Flicker in Cat Optic Nerve
233
impulses/set, superimposing this pattern upon the response to individual flashes of flicker. This induced impulse discharge will be described in more detail later. The response characteristics of the two types may be summarized as follows: the average impulse frequency of Type I varies as a function of flicker frequency, but that of Type II is independent of flicker frequency. Repetitive firing induced by flicker The average impulse frequency in Type I-cells was dependent on flicker frequency, as described above. When the flicker frequency was continuously and gradually changed around that frequency which elicited the maximum impulse average, some Type I-cells, which had a receptive field with a distinctive surround, showed impulses in addition to those bursts of impulses which corresponded to the individual flashes of flicker. When the flicker frequency was adjusted properly, these additional impulses increased and occurred midway in the interval between those bursts of impulses evoked by the individual flashes of flicker. We shall call this phenomenon induced activity. One example of induced activity in a Off-I unit is shown in Fig. 5. Figure 5A shows the impulse discharge patterns to flicker when the frequency of flicker was changed stepwise. Impulse discharges followed faithfully the flicker frequency up to 35 Hz, but when this unit was repeatedly stimulated by flicker at 14.1 Hz for about 10 set, induced firing occurred as shown in Fig. 5B. Induced activity was usually found to continue for as long as several tens of seconds and to be composed of regularly spaced impulses at about 200 Hz. These impulses were not time locked to the stimulus. During the induced activity, this cell continued to respond to individual flashes of flicker, overlapping the regularly spaced discharges. In the last stage of induced activity, impulses often fell out. This activity could be induced again by fmely re-tuning the flicker frequency. When 5icker stimulation was removed in the course of induced activity (Fig. 5C, arrow l), only the regularly spaced impulses remained, but the direct photic responses reappeared when flicker stimulation was recommenced (Fig. 5C, orrow 2). In Fig. 6, another example of induced activity is shown. In this On-I cell, induced activity was occurred when a flicker frequency was maintained at 30 Hz for longer than 10 sec. Induced activity, once it occurred, was not affected by a change of flicker frequency (Fig. 6B); it lasted for about 40 set after its initiation. The flicker frequency at which induced activity occurred, varied with the individual cell between about 10 and 30 Hz. Some cells showed induced activity only under the dark background condition. As is shown in Fig. 7A, an Off-I cell increased its impulse frequency to as high as 100 impulses/set at 20 Hz flicker under the light background condition, but it did not show induced activity. When the background light was removed, the maximum impulse frequency increased rapidly with flicker frequency and showed induced activity at 9.9 Hz flicker. Another Off-I cell showed induced activity under a variety of stimulus conditions (Fig. 7B). The flicker frequency at which induced activity occurred, was about the same (13*5-14.5 Hz) in every case. This cell showed some instability of the discharge pattern at low flicker frequencies under the condition of dark background and weaker stimulus intensity. It was occasionally observed that shadows which passed rapidly over the receptive field or that flicking the room light on and off initiated the induced activity when the tuned flicker frequency was not yet enough to induce the activity. Other kinds of periodic discharge patterns were also observed in the cells which did not
YOSHIROFUKADA AND HIDE-AKI SAITO
234
set
0
10
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40 30
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40 55 50 60
203 m set FIG. 6. A, Discharge patterns of an On-I to flicker stimulation. B, Induced activity of the same cell. It was induced by 30 Hz flicker, then flicker frequency was shifted to 20 Hz, 10 Hz
and 1 Hz, successively. Spike size; 2 mV. have such a strong surround as those which showed the induced activity. In Fig. 8A spontaneous periodic activity in the light adapted state is shown. Another exampie of periodic@ in maintained activity of an Off-I cell is shown in Fig. 8B. When the room light was turned off (Fig. 8B, arrow), the maintained discharge rate increased and some periodicity was observed {marked by a broken line on the right side of the records). Periodic firing in the maintained activity, similar to that described above, was not observed in the cell which exhibited induced activity.
Response to Flicker in Cat Optic Nerve
A
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g s 150a L
10
20
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40
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FLICKER
60
0
10
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FREQUENCV,
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FIG.7. Relation between average impulse frequency and flicker frequency for two Off-I cells which showed the induced activity. Stimulus condition as indicated. Other characteristics of the response to flicker
The CCF/intensity relation was also studied. The peak luminance of the light spot during the flicker was usually 1.94 x IO3 cd/m2. For some cells spot luminance was reduced with neutral density filters. Both Type I and Type II showed a definite tendency to lower the CCF as stimulus intensity was decreased (Fig. 9). This behavior was generally the same as that previously found with diffuse light stimuli in either dark or light adapted eyes (ENROTH, 1952; DODT and ENROTH, 1954; FUKADA et al., 1966) and with larger light spots (OGAWA et al., 1966). There has so far been no demonstrable difference between Type I and Type II -cells. The relation between CCF and maximum impulse frequency during flicker stimulation was studied next. With diffuse light stimuli, it had been previously shown (FUKADA et al., 1966) that all cells exhibited the same curvilinear functional relation expressed generally as: CCF = L [l-exp(-u.ZF,,,)] where ZF,,, = maximum impulse frequency (impulses/set) L = the upper limit of the CCF for a given set of stimulus conditions a = aconstant. In the present experiment, the CCF was plotted against the maximum impulse frequency as shown in Fig. 10. In all Type I-cells (circles and squares) there was a definite relation between CCF and maximum impulse frequency. A curve fitted to the observed points for Type I-cells, including those which showed induced activity, is shown in Fig. 10 by the broken line. This curve can be expressed as: CCF = 52 [l -exp(-0~0144ZF,,,,,)].
(1)
236
-
!OOmsec
This equation is of the same form as that obtained with diffuse light. It may als0 be noted that the #‘_ of Type I-ceils which have shown the induced activiQ a and El in Fig. 10) is tigber than the IF,, of tie otier Type I-cells (@ and 0) ; all of &em show more than 120 impuls~~sec. Type &cells (+ + -!-+) present a strong cantrast with Type I. They are divided into two groups and fall far away from the curve expressed by equatian (1). Therefore it is conceivable
Response to Flicker in Cat Optic Nerve
231
60 -
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log light intensity; zero correspond average luminan ce, 1.08 x lO’cd/m’. (O@@O)Represent On-I;(OOOO)Oti-r;(+++-t On-II. +
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FIO. 10. Relation between CCF and maximum impulse frequency for each type of cell. RepresentOn-I;(Wn H W)On-1 which showed induced activity; (0 0 0 0) O&I; (OOClO) Off-I which showed induced activity; (+ +++) On-II. Broken curve is drawn from equation 1 (see text). (~~~>
that the response characteristics of Type I and Type II to flicker stimulation are distinctly different. DISCUSSION The difference between Type I- and Type II-cells in response to flicker stimulation has been confirmed in this experiment. As the flicker frequency increases, the average impulse frequency in Type I-cells increases, passes through a maximum, and finally falls off. On the
other hand, the average impulse frequency in Type II-cells remains almost unchanged over a wide range of fficker frequencies, though many Type IE-cells can foilow even higher flicker frequencies than Type f-ceils. It is possible that Type If-cells may respond with the same average impufse frequency to a spot of tight if csn%ythe average fuminance is unchanged, Some Type II-cells exhibited labile responsiveness to flicker stimulation. These celis are not qualified to transfer temporal information, but they are competent for processing spatial information because their receptive field is small, centrally located and is most sensitive to stationary small objects. Type I-cells, in contrast with Type IX, are suitable far processing tem~o~l info~matio~~ as they ~~~~~t~~t~ the light stimulus with respect to time_ Concerning the relationship between CCF and conduction velocity, it is probable that almost all of the fibers which have been studied in the previous paper (FURADA et al., 1966) are Type I-cells, because under the condition of diffuse illumination Type II-cells respond oniy weakIy to flicker. The relation between CCF and conduction velocity obtained with a spot stimulus, was not as clear as that obtained with diffuse Iight. One of the probable reasons for this d%erence is that spatial summation over the whole receptive geld of a Type f-cell results in a smoothing out of the regional variations in responsiveness to flicker, MAFFEI (1968) has shown that the spatial average at the lateral geniculate body can achieve a smoothing and improve the signal-to-noise ratio in sine-wave responses. If the presence of this averaging effect is demonstrated in Type f-cells in the retina, it becomes more probable that the Type I-cell is suitable for deteoting a temporal change in the average intensity of light rather than the spatial difference in light intensity in its receptive Geld, Concerning the periodic activity in the visual system, a number of investigators have noted that periodic activities can be evoked by light flashes or affected by conditions of illumination (Dam and KKMURA,1963; CRAPPER and NQELL, 1963; BROWNand ROJAS, 1965; OGAWA, Bmo~ T_.mmz and ~~EAN~~
and L~vrcrc, 1966;
STEPGERG, 1966; STONEand FABXAN, 1966;
1967; PACRECO, BEAR arrd ERWN,
1968). Periodicity is also observed discharges (HEM and BORNXHE~, 1966; ~Efss, I%?; %XMXDT and CREUTZFELDT, 1968). It has been reported that there is an increased tendency to repetitive firing under barbiturate anaesthesia (KUFFLER,FITZHUGH and BARLOW,1957; DOTY and KIMURA,1963; BROWNand RCHAS,1965). In the present study cats were anaesthetized with Nembutal, Both the periodic bursts of spontaneous discharges in light (Fig. 8A) and the periodic@ observed when the room light was turned off (Fig, SB& seem r&ted to those phenomena already reported in the literature. However, in several respects, the induced activity is different from those phenomena previously reparted. The frequency of induced firing is very high (about 200 Hz), and it continues for as long as one minute with highly regular spike intervals. Once it has begun neither a change of flicker frequency nor withdrawal of the light stimulus has any elect on stopping the induced activity. Ganglion cells do not either change their ~s~ns~~enes~ to pbotic stimulation during the induced activity or show any sign of depression such as seen in the case of the retinal spreading depression (GOURAS,19%). Fifteen Type I-cells (On-I, 8; Off-I, 7) out of 32 Type I-cells which have exhibited a distinct surround response, have shown the induced activity. These are all cells which have reached a maximum impulse frequency of more than 120 impulses/see. Although a s~tem~t~c ~xarn~~at~o~ on the effect of drugs has not been attempted, an ad~t~on~ dose of Nembutaf (about fO m&kg) seemed to have no e&ct on induced activity. The above observations suggest to us that the induced activity may have some connection with the neuronal organization of the receptive field. The occurrence of the repetitive discharges of constant frequency in addition to transient bursts which follow in spontaneous
Response. to Flicker in Cat Optic Nerve
239
flickering light, may suggest that the ganglion cells receive long-lasting depolarizing inputs by a means different from the main path which conveys the flicker information through the retina, but no direct evidence of this interpretation has yet been obtained.
SUMMARY (1) The average impulse frequency in Type I-fibers (phasic type) increases, passes through a maximum, and finally falls off, as the flicker frequency increases. On the other hand, the average impulse frequency in Type II-fibers (tonic type) remains almost unchanged over a wide range of flicker frequencies. (2) In Type I, the highest flicker frequency at which the unit responds faithfully to individual fiashes (CCF), is correlated positively with conduction velocity. For Type II the CCF is not correlated with conduction velocity. Some Type II-units change responsiveness during flicker stimulation, and often stop the firing for several hundred msec. (3) In all Type I-fibers there is a definite relation between the CCF and the maximum impulse frequency, while in Type II the relation between them is not clear. (4) The majority of Type I-fibers which had a distinct antagonistic surround in their receptive field showed repetitive firing at high frequency (about 200 Hz) when the flicker frequency was adjusted properly around the frequency which elicited the maximum impulse frequency. (5) It is concluded that Type I is suitable for processing temporal information, while Type II is suitable_ for processing spatial information. Acknowledgnrenrs-The authors would like to thank Prof. K. TASAKI for his encouragement and for valuable suggestions on the manuscript. They are very grateful to Drs. A. C. NORTONand J. I. SIMPXINfor a critical reading of the manuscript.
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Abstract-The response characteristics of cat’s optic nerve fibers to flicker stimulation were investigated. As the flicker frequency increases, the average impulse frequency in Type Ifibers (phasic type) increases, passes through a maximum, and finally falls off. When the flicker frequency is adjusted properly, Type I-fiber which has a distinct surround in its receptive field shows a repetitive firing at high frequency (about 200 Hz). The average impulse frequency in Type II-fibers (tonic type) remains almost unchanged over a wide range- of flicker frequencies. R&urn&On &udie les caracteristiques de la reponse des fibres du nerf optique du chat a une stimulation papillotante. Quand la frtquence du papillotement augmente, la frequence moyenne des imp&ions des fibres du Type I (type phasique) augmente, passe par un maximum, et finalement diminue. Quand la frequence du papillotement est convenablement choisie, la fibre du Type I qui posdde un bord distinct dam son champ rkcepteur posskde une rkponse rbpktitive A grande fr&uence (vers 200 Hz). La frkquence moyenne d’impulsions des fibres du Type II (type tonique) reste presque sans changement dans un grand domaine defrequences de papillotement. Zusammenfassung-Es wurden die Antwortskennzeichen der Katzenoptikusfasern fiir Flimmerreize untersucht. Wenn sich die Flimmerfrequenz erhiiht, so steigt die mittlere Antwortsfrequenz der Fasem des Typus No. I (des phasischen Typus), erreicht einen Gipfel und vermindert sich am Ende. Wenn die Flimmerfrequenz richtig justiert ist. so zeigt Typus No. 1, welcher ein klares Umfeld in seinem Rezeptivfeld besitzt, eine wiederholte Hochfrequenzentladung (cu. 200 Hz). Die Mittelentladungsfrequenz der Fasem des Typus No. 2 (des ton&hen Typus) bleibt bei einem grossen Flimmerfrequenzbereich beinahe unverandert. aono~oH 3prftwrbHoro HepBa ~ounof B c~~~fyHauruo (hfe~5ruuotu~ii CB~T). Korga YBcTora ~e.nbzamiii ywcs, cpextuur 9acrora ribfnynbco~ BO~OKOHI-r0 mna (@ta~secrrnB rsm) riapacmer, npoXonnT Yew3 MaYCuMyM H, B KOHlre KOHUOB,naJB%T. EUIH YBcIy)Ta MeJtBKaHHHpel-yHB* pyeTUl TOYHO.TO BOlIOKHaI-r0 THlTa,KOTOpbteHMelOTB HX peuetTTHB.iiOMnone OnpeHeJteHHOe ~HB~aHBHoe OKp)meBHe, O6HapyZKHB;uoT nOBTOpBbIe pa3pKJ&t BbrcoKOti YacTOTbl (OKoHo 200 l%pn). GpeAHiul YiiCTOTZ3 HMITynBcoB BOnOKOHII-r0 TAna (TOHHYeCK& T%Hl) ocT8eTcII noYTB HeH3MeBHOftB npeAenaX IIIEpOKOrO JWaIW3OHB YXTOTbI MIXbKBiEii.
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