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Another new type of cat retinal ganglion cell?
ANOTHER NEW TYPE OF CAT RETINAL GANGLION CELL? Department of Psychology, Michigan State University. East Lansing. MI 48824. U.S.A. (Recrired 7 Aprii 1975;
in
revised form 22 Au+st 1975)
Abstract-A group of cat retinal ganglion cells. termed “triggered response cells”, responded to normal visual stimuli with elevations of their firing rates lasting tens or hundreds of seconds. These sells seem different from other cells whose maintained discharges undergo long-lasting changes. In many other respects “triggered response cells” resemble Y-type cells.
A number of reports have described cat retinal ganglion cells whose maintained discharge was unusual in one way or another. One such phenomenon was an oscillation of the rate of maintained discharge with a period of 60 set or more under conditions of dim background illumination (Rodieck and Smith, 1966; Ascoli and Maffei, 1964). More recently there have been several reports of stimulus “triggered”, long lasting, sustained elevations of the maintained discharge which may outlast the stimuius by tens or hundreds of seconds (Fukada and Saito, 1971; Saito and Fukada, 1973; Cleland and Levick, 1975). A possibly related result has also been described in L~~~~iis(Wasserman, 1968). Because these cells are encountered infrequently progress toward understand~g them has been slow. Several observations are described which might guide other investigators if they encounter similar cells. METHODS Preparation The anesthesia, surgical preparation, and immobilization of adult cats were essentially like those reported in a number of other reports by other investigators (Levick and Zacks, 1970; Cleland, Dubin and Levick, 1971). Following initial induction with ethyl chloride, anesthesia was continued with ether until the cephalic vein was cannulated. Then 1% thiamyl sodium (Surital) was administered i.v. as needed until all surgical procedures were completed. A tracheal cannula was installed to permit subsequent artificial ventilation. The cervical sympathetic trunk on the side of the eye to be recorded from was severed to aid ocular stability. A rectal thermistor was installed to permit monitoring and, through a feedback-regulated heating blanket. control of body temperature at 38-39’ C. The right eye was sutured to a steel ring to aid ocular stability and to provide support for the electrode manipulator (Cleland er al., 1971). The pupi was dilated with a mixture of 1% atropine and 25% neosynepherine. Following the surgical preparation the animal was paralyzed with an initial dose of 10 mgikg of Flaxedil, and maintained on 5 mgikg hr of Flaxedil in 6% glucose solution. Anesthesia was maintained from this point by a mixture of 70% nitrous oxide. 28.5% oxygen, and 15% carbon dioxide given at 34 strokesimin. The volume/stroke was determined from the graph by Kleinman and Radford (Harvard Apparatus, Millford. Mass.) and then multiplying that value by 1.5.
Retinal
recordinq
The basic aspects of the procedures
and apparatus used for extracellular recording from retinal ganglion cell bodies or their axons were base2 on proceduies similar to those described bv Levick and Zacks (1970). and Cleland et (II. (1971). Gla&.-insulated tungsten ‘micr&lectrodes, made as described by Levick (1972). were introduced into the right eye through a cannula which penetrated the globe just forward of the equator. A hydraulic micromanipulator and positioner were used to orient and advance the electrode onto the inner surface of the retina. Details of the ampli~cation and display ~angements using an a.c. coupled, high impedence preamplifier, cathode ray oscilloscope, and audio monitor were conventional. In addition the amplified signal was fed co a Schmitt trigger where the action potentials were used to initiate a pulse of standard amplitude and duration. This pulse was used to intensify the display of the action potential to verify triggering levels, as the input to a low-pass RC filter (Cleland er al., 1971) to provide a continuous record of mean firing rate on a chart recorder, and as the input to a LINC computer which was used to control stimulus presentation and to process the resulting trains of action potentials. On-line data processing The LINC computer was used to cumulate post-stimulus time histograms (Gerstein and Kiang, 1960). A useful variation of the post-stimulus time histogram consisted of a histogram representing the sums of the numbers of action potentials observed in each of 512 successive I-set intervals. This histogram could be used either to rqresent the maintained discharge in the absence of a stimulus or to represent responses to stimulation on a coarse time scale without requiring that the assumption of stationarity required for meaningful interpretation of multiple-sweep, post-stimulus time histograms be satisfied.
Stimuli Background illumination was provided either by an incandescent tungsten lamp run from the a.c. line. or. at lower luminances, another tungsten source operated from a regulated d.c. power supply. Stimuli were produced either by a bank of fluorescent tubes which were electronically gated on and off or by an incandescent projector controlled by an electromagnetically operated shutter. Luminances of the Bashed stimuli were controlled by neutral density filters and measured with a visual photometer (SEI, Ilford Ltd.).
OnI) csils bcirh on-center. &-surrounds wre studied in detail. One off-center cell uhich It-as examined onit cursorill; seemed to share the main feature of the cells described beio
The most si~j~cant property of rhe cells which I have encountered is their extended “response’. to very transient visual events. For example. a brief. barely perceptible (to the experimenter) shadow or diffuse increase in illumination may “trigger” an increase in firing rate which may persist for 100 set or more. The duration for which the increase in maintained discharge persists appears to be independent of the properties of the stimulus. For example, an intense flash does not seem to produce a greater or longer-lasting increase in the maintained discharge than does a weak flash. For this reason I will refer to these cells as ‘*triggered response cells”. Figure L.-l sho\vs the firing rate over a 512~set interval, during which time (a) a pair of ZOO-msec flashes was presented. {b) a flashlight was briefly shone on the ceiling above the animal and still later. (cf the Hash pair was repeated. The first present~~tion of the flash pair occurred when the firing rate was high. It evoked a transient increase in firin! for 1 or 2 sec. the expected response of a more ordinary ganglion cell to that stimulus. One hundred set later. after the maintained firing rate had dropped. the flashlight was briefly shone on the black ceiling above the animal. It trig gered a transient. high firing rate for a second or two, followed by a sustamed increase in firing lasting for about 100 sec. Somewhat later the paired flash stimulus was repeated. this time when the firing rate was low. Ir produced a high transient burst followed by over 150 set of sustained firing. Long-lasting changes in the maintained firing rate are also observed to occur spontaneously as is shown in Fig. If3 In other respects these “triggered response” cells appear to be very much like Y-type (also transient or Type-I) tEnroth-Cu~efl and Robson. 1966: Cleland er of.. 1971; Fukada. 1971: unpublished personal observation) on-center, off-surround retinal ganglion cells. in agreement bvith the reports of Cleland and Levick (1975). For example. n coarse, square-wave grating drifted through the receptive field modulates the firing rate of the cell at the rate of one burst per cycle of the grating drifting through the receptive field. With finer gratings the firing rate increases when the grating is moved, but without a modulation of the firing synchronized with the passage of individual bars through the receptive field. In addition the re-
‘This number is a berv rough approximation.
Often a
particular kind of cell ivas‘beinesought and cells ob\iously not of the appropriate type kvere immediately given up with no record kept of having encountered them.
TIME
;sec,
Fig. !. ..I’ 4 512~set iampls oi rhc xti\lt! of XI on-xnkr retinal ganglion cell. During this time a pair of X0-mssc Hashes. separated by about 1 ses. was pre%Hed twice. and a momzntxy. slight, oterall mcreas~ in background iuminance teas produced once ibv shining a flashlight on the black ceiling above the the animalr. Notice the brief response to the flash pair when they \cze presented with the maintained discharge relativelr Giph. and the long-ldstIng “response” u-hen the same stimuli ivere presented at ;I time Hhen the maintained discharge was low. 5: In this 312+x sample of the activit) of the same cell as ubobc. no stimuli were presented. The abrupt decrease and subsequent abrupt increase in ths maintained discharsc \verz ?pontancous.” (Cell C-102-1. runs dy; and 56. bdckqxmd luminance QOi8 ft-L.) i% artificial pupil was used because the natural pupil \r-as stable and open about 3 mm wide. The functional acuity was sooil. Bin widths were 1 WC.
sponses to stimuli at different locations in the receptive field and the effects of changes in background luminance were characteristic of k’ cells but not X cells as they have been observed in our taborator?; in studies of adaptation (unpublished observations). Triggered response cells dialer in at least three brays from cells previously described by Rodieck and Smith (1966) and Ascoli and Maffei (1964) (ahich I will refer to as Rodieck-type cells). First. Rodieck-type cells tended to ,eo throu@ regu!ar. cyclic oscillations of their maintained discharge. bvhereas the changes in maintained discharge observed in triggered response cells were much more irregular. ~~i~hou~h the irregularity is not apparent from the short sample of maintained actiritv shokvn in Fig. IS. it aas conspicuous when the miintained discharge was observed for a longer period of time.) Second. the Icvel of maintained tiring of the Rodieck-type cells was not shown to be influenced significantly by the presentation of suprathreshold stimuli. Final]?, when stimulus presentation was made contingent upon the rn~n~~ned fevel of firing the magnitude of the transient responses to brief stimuli behaved in opposite ways for the triggeredresponse cells and the Rodieck-type cells. For triggered response cells a greater change from the level of maintained firing occurred if the stimuli tvere presented at a time when the maintained discharge was ion than when the maintained levef of firing was high (Fig. 2). In a few cxlls which I hal-e looked at which seem to be Rodieck-type 41s the reverse ~1s true. Responses to stimuli presented when the maintained discharge rate was high were greater than TSsponses to the same stimuli when the mainrainzd discharge rate was IOLV.In fact. the magnitude of the response to a particular stimulus tended to increase rough14 in proportion to the increase in the mainrained firing rate (personai unpublished obserxxionl,
515
Another ne% type of cat retinal ganglion cell?
I
‘y_.:’ .-m::
1
O
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.,.,”
4’
, 0
.;.-
1
,_:.._-::
:::.: . . ..,,,; .’ ,._.
..,
-.:.
_
,=x.-
. . . . . -..t-..
: . .._. ., t.
.-_c;_
.
f&‘;
.
..:,.
2
1
high
+
200
SO0 400 TIME fnrroc)
800
1000
Fig. 2. A comparison of the averaged responses of a cell to the same stimulus (about 1.5 lo! units above threshold) presented either when the maintamed discharge was low. or when it was high. The peak tiring rate evoked by the stimulus was not signilicantly dependent upon the maintained discharge rate. (ClOj-1. runs 13 and 14. background luminance 16 ft-L. 3 mm artificial pupil. Histograms were cumulated usiy 20 rcpetitinw of the stimulus at the rate of one repetttlon per 3 WC \LII~ a I-mwc bin Kidth.1
Thus. these do not seem to be the same as Rodiecktype cells. These cells do seem to be like those described by Cleland and Levick (1975). Fukada and Saito (1971) and Saito and Fukada (1973) in some ways, but different in others. They are similar in that the sustained or “induced” discharge can be elicited by the presentation of a stimulus. only Y or transient type Cells seem to exhibit this behavior. and the increase in firing produced by a stimulus seems to be reduced when stimulus presentation occurs during a time of high maintained discharge. However there are also several differences between some of my observations and those previously reported by others. Most striking is the difference between the rate of induced firing I have observed and that reported by others. Earlier reports described induced firing rates of around 200 sec. The most recent report (Cleland and Levick, 1975) offers evidence for the existence of a spikegenerating focus. which is responsible for the high rate of firyng. being located somewhere along the axon of the cell. The cells which I have observed have typicallr; been induced to fire continuously at 30-80&c, with a normal maintained discharge below lO,&ec.Although the levels of the maintained discharge as well as the rate of discharge which can be triggered are somewhat dependent on background luminance, I have never encountered an induced discharge as high as 2O@sec. Whereas previous investigators used repetitive stimuli (14 ‘set flashes. rapid alternative presentation of the black and white sides of a disc), in these experiments intense singte flashes (about I.5 log units above threshold) or very weak, diffuse illumination sufficed to induce elevations of firing in the cells reported here. Furthermore. in ail of the cells I have seen which could be triggered similar changes were observed to occur spontaneously. The spontaneous cessation of induced activity is usually very abrupt. suggesting that if the rate falls below some critical level it will no longer persist. Similarly it appears that if the rate exceeds a criterion level. either because of the presentation of a stimulus or because of a spontaneous. extreme fluctuation of the maintained discharge, then a high rate of firing may result.
Rodieck-type fluctuations in maintained discharge tend to lx seen in total darkness. Barlow and Levick (1969) reported similar fluctuations especially with backgrounds in the range just above lo-’ cd. m’ with a 3-mm-dia artificial pupil. Although they report that they believe these oscillations tended to occur when the condition of the eye or the whole preparation was in doubt. they also report fluctuations occurring when they could find no fauit with the preparation. These were observed infrequentiy.and the magnitude of the fluctuations were “relatively minor”. This raises the question whether the triggered respong ceils are the sign of a preparation in distress. Because no’major physiological variables were monitored in the course of these experiments I cannot offer any direct evidence. However. there did not seem to be any tendency to see these cells late in the experiment (which usually last 18-72 hr) insofar as one can tell w_ith six cells. In some cases perfectly normal appearmg cells ivere observed at virtuallv the samqretinal locus fo~lo~~,in~recording from a triggered response cell. As more and more detailed distinctions are made between groups of retinal gan.glion ceils it becomes increasingly important to consider the significance of these distinctions. Should one seriously consider six cells sharing an unusual property’? Although they might indeed be an uninteresting artifact. there are several reasons why they should not be dismissed out of hand. First, the relative frequency with which they occur in the retina might be higher than their occurrence in the sample because of electrode sampling biases (Stone, 1973; Levick and Cleland. 1974). Second. even though they may occur ~frequently in the retina. few of them may be needed to carry out the particular role they play in information processin+. Finally. even if they are a physiological anomaly theu particular abnormality may help to reveal important properties which contribute to the function of normal cells. Acknotrled~ments-I gratefully acknowledge a most constructive review by an anonymous reviewer for &ion Resear& This research was conducted under &SF Research Grant No. B1MS?2-01793A02 REFERENCES
Ascoli D. and ;MaKeiL. (1964) Slow periodicity in the dark discharge of retinal units. Erperi&ria 20. f26. Barlow H. B. and Levick W. R. 11969) Changes in the maintained discharge with adaptation level h the cat retina. J. Ph_~siol.,Land. 202, 699-718. Cleland B. G., Dubin M. W. and Levick W. R. (1971) Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. J. Pkysiol.. Land. 217, 473-496. Cleland B. G. and Levick W. R. t 1974af Brisk and sluggish concentrically organized ganglion cells in the cat’s retina J. Pk.&i.. Land. 240, 4X-456. Cleland B. G. and Levick W. R. (1947b) Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. J. Pk_Wbl.. Lord. 240. 457-492.
Cleland B. G. and Levick W. R. (1975) The nature of the “induced” discharge of cat retinal ganglion cells. J. Pk,v siol., Lord. 244, 6OP-61 P. Enroth-Cugell C. and Robson J. G. (1966) The contrast sensitivity of retinal ganglion cells of the cat. 1. Pkysiol.. Lmrd.
187, 5 17-S.
JAMESL. ZAC~S Fukada Y. 11971) Receptive held organization of cat optic nerve fibers with special reference to conduction velocity. Cision Rex 1t, m-?‘6. __ Fukada Y. and Saito H. (1971) The relationship between response characteristics to flicker stimulation and receptive field organization in the cat’s optic nerve fibers. Msion Rrs. 11. 227-240. Gerstein L. and Kiang Y. S. (1960) An approach to the quantitative analysis of electrophysiological data from single neurons. Biophps. J. 1, 15-X Kuffler S. W. (1953) Discharge patterns and functional organization of mammalian retina. J. Newophysiol. 16, 37-68. Levick W. R. (1972) Another tungsten microelectrode. Met/. Bid. Engng 10. 510-515.
Levxk W. R. and Cleland B. G. I 1974) Selecrn ity of mtcr+ electrodes in recordings from cat retinal ganglion cells. J. .Veurophniol. 37. 1387-l 393. Levick W. R. and Zacks 1. L. (1970) Responses of cat retinal ganglion cells to brief tlashes of light. J. Ph~~iol.. Land. 106, 677-700. Rodieck R. W. and Smith P. S. (1966) Slow dark discharge rhythms of cat retinal ganglion cells. J. Neuroph~siol. 29. 942-953. Saito H. and Fukada Y. (1973) Repetitive tiring of the cat‘s retinal ganglion cells. Cision Res. 13. 263-270. Stone J. (1973) Sampling properties of minoelectrodes assessed in the cat’s retina. J. Sertrophysiol. 36. 1071-1079. Wasserman G. S. (1968) Persistent effects of brief stimuli interacting with the hyperpolarizing response. Physiol. & Behrrc. 3, 835-817.
in
revised form 22 Au+st 1975)
Abstract-A group of cat retinal ganglion cells. termed “triggered response cells”, responded to normal visual stimuli with elevations of their firing rates lasting tens or hundreds of seconds. These sells seem different from other cells whose maintained discharges undergo long-lasting changes. In many other respects “triggered response cells” resemble Y-type cells.
A number of reports have described cat retinal ganglion cells whose maintained discharge was unusual in one way or another. One such phenomenon was an oscillation of the rate of maintained discharge with a period of 60 set or more under conditions of dim background illumination (Rodieck and Smith, 1966; Ascoli and Maffei, 1964). More recently there have been several reports of stimulus “triggered”, long lasting, sustained elevations of the maintained discharge which may outlast the stimuius by tens or hundreds of seconds (Fukada and Saito, 1971; Saito and Fukada, 1973; Cleland and Levick, 1975). A possibly related result has also been described in L~~~~iis(Wasserman, 1968). Because these cells are encountered infrequently progress toward understand~g them has been slow. Several observations are described which might guide other investigators if they encounter similar cells. METHODS Preparation The anesthesia, surgical preparation, and immobilization of adult cats were essentially like those reported in a number of other reports by other investigators (Levick and Zacks, 1970; Cleland, Dubin and Levick, 1971). Following initial induction with ethyl chloride, anesthesia was continued with ether until the cephalic vein was cannulated. Then 1% thiamyl sodium (Surital) was administered i.v. as needed until all surgical procedures were completed. A tracheal cannula was installed to permit subsequent artificial ventilation. The cervical sympathetic trunk on the side of the eye to be recorded from was severed to aid ocular stability. A rectal thermistor was installed to permit monitoring and, through a feedback-regulated heating blanket. control of body temperature at 38-39’ C. The right eye was sutured to a steel ring to aid ocular stability and to provide support for the electrode manipulator (Cleland er al., 1971). The pupi was dilated with a mixture of 1% atropine and 25% neosynepherine. Following the surgical preparation the animal was paralyzed with an initial dose of 10 mgikg of Flaxedil, and maintained on 5 mgikg hr of Flaxedil in 6% glucose solution. Anesthesia was maintained from this point by a mixture of 70% nitrous oxide. 28.5% oxygen, and 15% carbon dioxide given at 34 strokesimin. The volume/stroke was determined from the graph by Kleinman and Radford (Harvard Apparatus, Millford. Mass.) and then multiplying that value by 1.5.
Retinal
recordinq
The basic aspects of the procedures
and apparatus used for extracellular recording from retinal ganglion cell bodies or their axons were base2 on proceduies similar to those described bv Levick and Zacks (1970). and Cleland et (II. (1971). Gla&.-insulated tungsten ‘micr&lectrodes, made as described by Levick (1972). were introduced into the right eye through a cannula which penetrated the globe just forward of the equator. A hydraulic micromanipulator and positioner were used to orient and advance the electrode onto the inner surface of the retina. Details of the ampli~cation and display ~angements using an a.c. coupled, high impedence preamplifier, cathode ray oscilloscope, and audio monitor were conventional. In addition the amplified signal was fed co a Schmitt trigger where the action potentials were used to initiate a pulse of standard amplitude and duration. This pulse was used to intensify the display of the action potential to verify triggering levels, as the input to a low-pass RC filter (Cleland er al., 1971) to provide a continuous record of mean firing rate on a chart recorder, and as the input to a LINC computer which was used to control stimulus presentation and to process the resulting trains of action potentials. On-line data processing The LINC computer was used to cumulate post-stimulus time histograms (Gerstein and Kiang, 1960). A useful variation of the post-stimulus time histogram consisted of a histogram representing the sums of the numbers of action potentials observed in each of 512 successive I-set intervals. This histogram could be used either to rqresent the maintained discharge in the absence of a stimulus or to represent responses to stimulation on a coarse time scale without requiring that the assumption of stationarity required for meaningful interpretation of multiple-sweep, post-stimulus time histograms be satisfied.
Stimuli Background illumination was provided either by an incandescent tungsten lamp run from the a.c. line. or. at lower luminances, another tungsten source operated from a regulated d.c. power supply. Stimuli were produced either by a bank of fluorescent tubes which were electronically gated on and off or by an incandescent projector controlled by an electromagnetically operated shutter. Luminances of the Bashed stimuli were controlled by neutral density filters and measured with a visual photometer (SEI, Ilford Ltd.).
OnI) csils bcirh on-center. &-surrounds wre studied in detail. One off-center cell uhich It-as examined onit cursorill; seemed to share the main feature of the cells described beio
The most si~j~cant property of rhe cells which I have encountered is their extended “response’. to very transient visual events. For example. a brief. barely perceptible (to the experimenter) shadow or diffuse increase in illumination may “trigger” an increase in firing rate which may persist for 100 set or more. The duration for which the increase in maintained discharge persists appears to be independent of the properties of the stimulus. For example, an intense flash does not seem to produce a greater or longer-lasting increase in the maintained discharge than does a weak flash. For this reason I will refer to these cells as ‘*triggered response cells”. Figure L.-l sho\vs the firing rate over a 512~set interval, during which time (a) a pair of ZOO-msec flashes was presented. {b) a flashlight was briefly shone on the ceiling above the animal and still later. (cf the Hash pair was repeated. The first present~~tion of the flash pair occurred when the firing rate was high. It evoked a transient increase in firin! for 1 or 2 sec. the expected response of a more ordinary ganglion cell to that stimulus. One hundred set later. after the maintained firing rate had dropped. the flashlight was briefly shone on the black ceiling above the animal. It trig gered a transient. high firing rate for a second or two, followed by a sustamed increase in firing lasting for about 100 sec. Somewhat later the paired flash stimulus was repeated. this time when the firing rate was low. Ir produced a high transient burst followed by over 150 set of sustained firing. Long-lasting changes in the maintained firing rate are also observed to occur spontaneously as is shown in Fig. If3 In other respects these “triggered response” cells appear to be very much like Y-type (also transient or Type-I) tEnroth-Cu~efl and Robson. 1966: Cleland er of.. 1971; Fukada. 1971: unpublished personal observation) on-center, off-surround retinal ganglion cells. in agreement bvith the reports of Cleland and Levick (1975). For example. n coarse, square-wave grating drifted through the receptive field modulates the firing rate of the cell at the rate of one burst per cycle of the grating drifting through the receptive field. With finer gratings the firing rate increases when the grating is moved, but without a modulation of the firing synchronized with the passage of individual bars through the receptive field. In addition the re-
‘This number is a berv rough approximation.
Often a
particular kind of cell ivas‘beinesought and cells ob\iously not of the appropriate type kvere immediately given up with no record kept of having encountered them.
TIME
;sec,
Fig. !. ..I’ 4 512~set iampls oi rhc xti\lt! of XI on-xnkr retinal ganglion cell. During this time a pair of X0-mssc Hashes. separated by about 1 ses. was pre%Hed twice. and a momzntxy. slight, oterall mcreas~ in background iuminance teas produced once ibv shining a flashlight on the black ceiling above the the animalr. Notice the brief response to the flash pair when they \cze presented with the maintained discharge relativelr Giph. and the long-ldstIng “response” u-hen the same stimuli ivere presented at ;I time Hhen the maintained discharge was low. 5: In this 312+x sample of the activit) of the same cell as ubobc. no stimuli were presented. The abrupt decrease and subsequent abrupt increase in ths maintained discharsc \verz ?pontancous.” (Cell C-102-1. runs dy; and 56. bdckqxmd luminance QOi8 ft-L.) i% artificial pupil was used because the natural pupil \r-as stable and open about 3 mm wide. The functional acuity was sooil. Bin widths were 1 WC.
sponses to stimuli at different locations in the receptive field and the effects of changes in background luminance were characteristic of k’ cells but not X cells as they have been observed in our taborator?; in studies of adaptation (unpublished observations). Triggered response cells dialer in at least three brays from cells previously described by Rodieck and Smith (1966) and Ascoli and Maffei (1964) (ahich I will refer to as Rodieck-type cells). First. Rodieck-type cells tended to ,eo throu@ regu!ar. cyclic oscillations of their maintained discharge. bvhereas the changes in maintained discharge observed in triggered response cells were much more irregular. ~~i~hou~h the irregularity is not apparent from the short sample of maintained actiritv shokvn in Fig. IS. it aas conspicuous when the miintained discharge was observed for a longer period of time.) Second. the Icvel of maintained tiring of the Rodieck-type cells was not shown to be influenced significantly by the presentation of suprathreshold stimuli. Final]?, when stimulus presentation was made contingent upon the rn~n~~ned fevel of firing the magnitude of the transient responses to brief stimuli behaved in opposite ways for the triggeredresponse cells and the Rodieck-type cells. For triggered response cells a greater change from the level of maintained firing occurred if the stimuli tvere presented at a time when the maintained discharge was ion than when the maintained levef of firing was high (Fig. 2). In a few cxlls which I hal-e looked at which seem to be Rodieck-type 41s the reverse ~1s true. Responses to stimuli presented when the maintained discharge rate was high were greater than TSsponses to the same stimuli when the mainrainzd discharge rate was IOLV.In fact. the magnitude of the response to a particular stimulus tended to increase rough14 in proportion to the increase in the mainrained firing rate (personai unpublished obserxxionl,
515
Another ne% type of cat retinal ganglion cell?
I
‘y_.:’ .-m::
1
O
.y.;:“__:.:__-;;; ..: .
.,.,”
4’
, 0
.;.-
1
,_:.._-::
:::.: . . ..,,,; .’ ,._.
..,
-.:.
_
,=x.-
. . . . . -..t-..
: . .._. ., t.
.-_c;_
.
f&‘;
.
..:,.
2
1
high
+
200
SO0 400 TIME fnrroc)
800
1000
Fig. 2. A comparison of the averaged responses of a cell to the same stimulus (about 1.5 lo! units above threshold) presented either when the maintamed discharge was low. or when it was high. The peak tiring rate evoked by the stimulus was not signilicantly dependent upon the maintained discharge rate. (ClOj-1. runs 13 and 14. background luminance 16 ft-L. 3 mm artificial pupil. Histograms were cumulated usiy 20 rcpetitinw of the stimulus at the rate of one repetttlon per 3 WC \LII~ a I-mwc bin Kidth.1
Thus. these do not seem to be the same as Rodiecktype cells. These cells do seem to be like those described by Cleland and Levick (1975). Fukada and Saito (1971) and Saito and Fukada (1973) in some ways, but different in others. They are similar in that the sustained or “induced” discharge can be elicited by the presentation of a stimulus. only Y or transient type Cells seem to exhibit this behavior. and the increase in firing produced by a stimulus seems to be reduced when stimulus presentation occurs during a time of high maintained discharge. However there are also several differences between some of my observations and those previously reported by others. Most striking is the difference between the rate of induced firing I have observed and that reported by others. Earlier reports described induced firing rates of around 200 sec. The most recent report (Cleland and Levick, 1975) offers evidence for the existence of a spikegenerating focus. which is responsible for the high rate of firyng. being located somewhere along the axon of the cell. The cells which I have observed have typicallr; been induced to fire continuously at 30-80&c, with a normal maintained discharge below lO,&ec.Although the levels of the maintained discharge as well as the rate of discharge which can be triggered are somewhat dependent on background luminance, I have never encountered an induced discharge as high as 2O@sec. Whereas previous investigators used repetitive stimuli (14 ‘set flashes. rapid alternative presentation of the black and white sides of a disc), in these experiments intense singte flashes (about I.5 log units above threshold) or very weak, diffuse illumination sufficed to induce elevations of firing in the cells reported here. Furthermore. in ail of the cells I have seen which could be triggered similar changes were observed to occur spontaneously. The spontaneous cessation of induced activity is usually very abrupt. suggesting that if the rate falls below some critical level it will no longer persist. Similarly it appears that if the rate exceeds a criterion level. either because of the presentation of a stimulus or because of a spontaneous. extreme fluctuation of the maintained discharge, then a high rate of firing may result.
Rodieck-type fluctuations in maintained discharge tend to lx seen in total darkness. Barlow and Levick (1969) reported similar fluctuations especially with backgrounds in the range just above lo-’ cd. m’ with a 3-mm-dia artificial pupil. Although they report that they believe these oscillations tended to occur when the condition of the eye or the whole preparation was in doubt. they also report fluctuations occurring when they could find no fauit with the preparation. These were observed infrequentiy.and the magnitude of the fluctuations were “relatively minor”. This raises the question whether the triggered respong ceils are the sign of a preparation in distress. Because no’major physiological variables were monitored in the course of these experiments I cannot offer any direct evidence. However. there did not seem to be any tendency to see these cells late in the experiment (which usually last 18-72 hr) insofar as one can tell w_ith six cells. In some cases perfectly normal appearmg cells ivere observed at virtuallv the samqretinal locus fo~lo~~,in~recording from a triggered response cell. As more and more detailed distinctions are made between groups of retinal gan.glion ceils it becomes increasingly important to consider the significance of these distinctions. Should one seriously consider six cells sharing an unusual property’? Although they might indeed be an uninteresting artifact. there are several reasons why they should not be dismissed out of hand. First, the relative frequency with which they occur in the retina might be higher than their occurrence in the sample because of electrode sampling biases (Stone, 1973; Levick and Cleland. 1974). Second. even though they may occur ~frequently in the retina. few of them may be needed to carry out the particular role they play in information processin+. Finally. even if they are a physiological anomaly theu particular abnormality may help to reveal important properties which contribute to the function of normal cells. Acknotrled~ments-I gratefully acknowledge a most constructive review by an anonymous reviewer for &ion Resear& This research was conducted under &SF Research Grant No. B1MS?2-01793A02 REFERENCES
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