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Turtle and catfish horizontal cells show different dynamic response
TURTLE AND CATFISH HORIZONTAL CELLS SHOW DIFFERENT DYNAMIC RESPONSE *I . KEN-ICHI NAKA and MASAXORI SAKCRASAGA’ RICHARD L. CHAPPELL National
Institute
for Basic Biology,
Okazaki.
(Receiced 30 November 1982: in rerised firm
44-l Japan 9 rMa.v 1983)
Abstract-Horizontal cell responses of catfish and turtle have been found to differ in a characteristic way. These characteristics established by white-noise analysis show that the impulse response (first order Wiener kernel) of the catfish horizontal cell has a substantially shorter latency as well as peak response time than that of the turtle. The turtle horizontal cell. on the other hand, has a dynamic gain which is twice that of the catfsh. Since these differences were established under conditions of ambient illumination, they may be expected to be functionally important in the visual experience of the animals under normal environmental conditions. Catfish
Turtle
Kernels
Incremental sensitivity
750 photodiode. Results were analyzed as power spectra, probability density functions (PDFs), and first order (Wiener) kernels (Marmarelis and Marmarelis, 1978). Analysis was accomplished off-line by a software system, STAR, developed by N. Mumata of Rikei Computer Co., Tokyo and Y. Ando of NIBB. Details of algorithms will be published elsewhere (Sakuranaga, 1984, in preparation). To facilitate response comparisons, we chose a pair of responses for which the stimuli had almost identical power spectra. Figure l(A) shows the power spectra of the input light stimuli and of the responses from the horizontal cells for the turtle (dashed lines) and catfish (solid lines). Both inputs had a flat power spectrum from near DC to 70 Hz and the response spectra were also very similar with their cutoff frequency at around IOHz. The probability density functions (PDFs) for the responses are shown in Fig. l(B). The two PDFs had a bell-shaped distribution which reflects the Gaussian distribution of the inputs’ PDFs and the cells’ linear response. The peak-topeak modulation was almost 20mV for the turtle response (dashed line) but was less than l0mV for the catfish response (solid line): although they had similar frequency response characteristics, the turtle horizontal cells responded more vigorously to the white-noise modulation of the input stimulus. The first order kernels obtained from these responses are shown in Fig. 2(A). The kernels are the response of the cells to an impulse input superposed on the mean of the white-noise stimulus. In a linear or quasi-linear system, the kernel’s amplitude is the system’s incremental sensitivity (Naka er al., 1979). In catfish, as well as in turtle, the horizontal cell response evoked by white-noise stimulus was linear (Marmarelis and Naka. 1973). In the turtle the linearity was held even though the peak-to-peak excursion of response was more than 20 mV as seen
In the course of our studies of the catfish and turtle retinas, we have noted a consistent difference between the responses from their horizontal cells. In this short report, we present results pertinent to this finding. The eyecup preparations of the channel catfish, Icrcllrrrrrs puncrutus, and the red-eared turtle, Pseudemys scripru elegans, used in these studies were maintained in a moist chamber into which fresh oxygen was. continuously supplied. We used a travelling random grating to measure the receptive field size (Davis and Naka, 1980). In the turtle experiments two simultaneous recordings were made from luminosity horizontal cells separated by about 0.4 mm. Comparison of the simultaneously recorded receptive field profiles enabled us to identify small (L2-HC) and large (LI-HC) field responses (Simon, 1973; Lam, 1976). Results described here were based on the small field responses. Catfish data were from the horizontal cell soma. In both cases, the horizontal cell bodies receive mainly the red cone inputs (Simon, 1973; Naka, 1969). Experiments were performed at a room temperature of 20°C. Step-evoked responses from the turtle horizontal cells had the characteristic initial peak followed by a plateau phase. The responses were very similar to those seen by other authors (Cervetto and MacNichol, 1972). The stimulus used was whitenoise modulated light with a mean irradiance of Z.O~W/cm’ at the retina [log neutral density filters were used to attenuate this beam to obtain the data for Fig. 2(B)]. The stimulus covered the entire surface of the retina. Electrophysiological recording was conventional. Intracellular responses were tape recorded along with the input signal monitored simultaneously by a United Detector Technology UDT
*Present
address:
X.Y. 10021. U.S.A. I I? Japan.
‘Hunter and ‘Nippon
Horizontal cells
College. 695 Park Ave.. Medical School, Tokyo,
II7
R. k
I3
I
Frequency
CH.APPCLL
!CC
Hz
t’r d
the possibilities of our results havmg been due to seasonal factors or conditions of speclmcns. Over the entire range. the impulse response :ti the cattish horizontal cell to an incremental stimulus has substantially shorter peak response times than that of the turtle. The curves are non-parallel 30 that a simple shift along the lop intensity axis as might be suggested for the difTerencr In the (static) sensitivit;. of the two retinas would not account for the difference. Furthermore. one would expect the maximal eytursion of the response in the turtle to be smaller. IIO: larger, than that of the catfish horizontal cells If only that wx involved. In fact. for a given impulse stimulus. since the amplitude of the response in the turtle horizontal cells is twice that of the cattish [shown h> the PDFs
B
-15mV
Fig. I(A). Power spectra of the two stimulus inputs and of the responses evoked. Data for the turtle experiment are in dashed lines and those for catfish in solid lines. Power (20 decibels per division) of the inputs, plotted as a function of frequency (Hz), is nearly flat up to 70 Hz. (B) Probability density functions (PDFs) for the responses whose power spectra are shown in l(A) above. The ordinates for the two distributions have been scaled so that the peaks of the distributions overlap. Mean of the curves was the average level of hyperpolarization around which modulation was superposed. The two curves were laterally displaced so that their means coincided. The excursion amplitude for the turtle was twice that observed in the catfish.
in Fig. l(B) (Naka et al., 1982). This linearity is consistent with the observations made by Tranchina
ef al. (1981) with the turtle horizontal cells but is in contrast with those made by Baylor and Hodgkin (1973) with the step-evoked receptor response. We note that (1) both kernels had almost identical waveforms as we would expect from the power spectra of Fig. l(A) and (2) there was a fixed delay of 20 msec between catfish and turtle kernels. Comparable data obtained over 4 log units of mean intensity (by using log neutral density filters to attenuate the beam without altering the depth of modulation of the stimulus) is summarized in the graph of Fig. 2(B). Turtle data, in circles, were an average of 7 complete runs whereas catfish data, in triangles, were an average of 6 complete runs. (In the figure legends standard deviations are given.) These data were obtained over a period of I year excluding
E
Fig. 2(A). First order Wiener kernels obtained from analysis of responses to the white noise stimuli. Kernels were normalized: one division on the ordinate is 9 mV/)c W/see for catfish and I7 rnV,p Wisec for turtle. Physiologically these kernels represent the imputse response of the eells superposed on the steady hyperpoiarization. The cattish horizontal cell impulse response (solid line) has a waveform almost identical with that from the turtle (dashed line). The catfish response is faster with a delay of 20 msec between the catfish and turtle kernels. Mean square errors (MSEs) were less than 101; for each. As one would exoect from the PDFs in Fig. I(bi the amplitude of the turtle kernel was twice that of the catfish kernel. (B) Peak response time for turtle and catfish. Peak response times for catfish (triangtes) and turtle (circles) first order kernels are plotted as a function of mean intensity. The incident beams were attenuated using fog neutral density filters in order to obtain the data at additional mean intensities with the same depth of modulation of the stimulus. The impulse response of catfish ceits was consistently faster than that of the turtle over the entire range investigated. The maximal irradiance was 2 PWfcm’. Turtle data was a mean of 7 runs and catfish data was a mean of 6 runs, each run covering a range of 3 log units. Standard deviations (from the brighter to dimmer means) were 1.3. 3.8, 7.5 and 6.1 for turtle and 4.9. 5.2. 5.8 and 12.3 for catfish points.
Kernel
responses
chardcterlze
in Fig. i(B) and scales of the kernals given in Fig. 2(A). legend]. the turtle horizontal cells will have hyperpolarized by almost the same amount as those of the catfish at the time the cattish horizontal cells reach their peak and begin to repoiarize. The turtle cells will go on to reach a peak which is twice as great as that reached by the catfish ceils although this results in prolonging the response. The cattish peak response time curve of Fig. 3(B) is almost identical vvith a plot of the time to half amplitude of the turtle kernels at each intensity. It appears, then, that compared with the turtle, the catfish horizontal cell response latency is signilicantly shorter but the response’s dynamic gain is half that of the turtle response. In summary, our results have demonstrated that turtle horizontal cells had a larger dynamic (incremental) gain than catfish cells but that this gain was concomitant with a longer delay and peak response time. Here we note that the step evoked response from turtle cells had the well documented initial (hyperpolarizing) peak followed by a plateau whereas catfish horizontal cells produced an almost square-looking response. In both retinas the horizontal cells from which the present results were obtained receive direct synaptic input from the receptors. The longer delay of the turtle horizontal cells might have been due to longer delay in the turtle receptors or might have been due to longer transmission delay between the receptor and horizontal cells or a combination of both. Additional experiments are apparently needed to explore further these interesting observations. We have shown in this report that there
119
differences
are subtle but functionally important diRerences between the horizontal cell responses from ditTerent species. Acl;nu~~,lelf~ernenl-Supported partly bq NIH Grants EY00777 and EY-01897. REFEREXES
Baylor
D. A. and Hodgkin A. L. (1973) Detection and resolution of casual stimuli by turtle photoreceptors. J. Phssiof.. Lord. 234. 163-198. Cervetto L. and .MacNichol E. F. Jr (1972) Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Scirvrcr 178. 367-768. Davis G. W. and Naka K.-I. (1980) Spatial organization of catfish retinal neurons. I. Single- and random-bar stimulation J, Newophysiof. 43. 807-83 I. Lam T. D. (1976) Spatial properties of horizontal cell responses in the turtle retina. J. Phy.riof.. Lund. 263. 239-235. Marmarelis P. 2. and Marmarelis V. Z. (1978) rlnu!,~si.s 01‘ Ph~~ioli~#icaf S?:rtetm: Whfte-noi.se ~pp~oij~t~. Plenum, New York. Marmarelis P. Z. and Naka K.-i. (1973) Noniinrar analysis and synthesis of receptive-field responses in the catfish retina. II. One-input white-noise analysis. J. ,Veurophysiof. 36, 634648. Naka K.-l. (1969) Computer assisted analysis of Spotentials. ~j~~~~~. J. 9, 845-859. Naka K.-I., Chan R. Y. and Yasui S. (i97Y) Adaptation in catfish retina. .!. Neurophysiol. 42, 441454. Naka K.-l.. Sakuranaga M. and Chappell R. L. (1982) Wiener analysis of turtle horizontal cells. Blamed. Res. (Suppf.) 3, 131-136. Simon E. J. (1973) Two types of luminosity hortzontal cells in the retina oi the turtle. J. Plr~~io(., Land. 230. 199-21 I. Tranchina I)., Gordon J., Shapley R. and Toyoda J. (1981) Linear information prozssing in the retina: A study of horizontal cell responses. Proc. nn/n. Acnd Sci. U.S.A. 78, 6540-6542.
Institute
for Basic Biology,
Okazaki.
(Receiced 30 November 1982: in rerised firm
44-l Japan 9 rMa.v 1983)
Abstract-Horizontal cell responses of catfish and turtle have been found to differ in a characteristic way. These characteristics established by white-noise analysis show that the impulse response (first order Wiener kernel) of the catfish horizontal cell has a substantially shorter latency as well as peak response time than that of the turtle. The turtle horizontal cell. on the other hand, has a dynamic gain which is twice that of the catfsh. Since these differences were established under conditions of ambient illumination, they may be expected to be functionally important in the visual experience of the animals under normal environmental conditions. Catfish
Turtle
Kernels
Incremental sensitivity
750 photodiode. Results were analyzed as power spectra, probability density functions (PDFs), and first order (Wiener) kernels (Marmarelis and Marmarelis, 1978). Analysis was accomplished off-line by a software system, STAR, developed by N. Mumata of Rikei Computer Co., Tokyo and Y. Ando of NIBB. Details of algorithms will be published elsewhere (Sakuranaga, 1984, in preparation). To facilitate response comparisons, we chose a pair of responses for which the stimuli had almost identical power spectra. Figure l(A) shows the power spectra of the input light stimuli and of the responses from the horizontal cells for the turtle (dashed lines) and catfish (solid lines). Both inputs had a flat power spectrum from near DC to 70 Hz and the response spectra were also very similar with their cutoff frequency at around IOHz. The probability density functions (PDFs) for the responses are shown in Fig. l(B). The two PDFs had a bell-shaped distribution which reflects the Gaussian distribution of the inputs’ PDFs and the cells’ linear response. The peak-topeak modulation was almost 20mV for the turtle response (dashed line) but was less than l0mV for the catfish response (solid line): although they had similar frequency response characteristics, the turtle horizontal cells responded more vigorously to the white-noise modulation of the input stimulus. The first order kernels obtained from these responses are shown in Fig. 2(A). The kernels are the response of the cells to an impulse input superposed on the mean of the white-noise stimulus. In a linear or quasi-linear system, the kernel’s amplitude is the system’s incremental sensitivity (Naka er al., 1979). In catfish, as well as in turtle, the horizontal cell response evoked by white-noise stimulus was linear (Marmarelis and Naka. 1973). In the turtle the linearity was held even though the peak-to-peak excursion of response was more than 20 mV as seen
In the course of our studies of the catfish and turtle retinas, we have noted a consistent difference between the responses from their horizontal cells. In this short report, we present results pertinent to this finding. The eyecup preparations of the channel catfish, Icrcllrrrrrs puncrutus, and the red-eared turtle, Pseudemys scripru elegans, used in these studies were maintained in a moist chamber into which fresh oxygen was. continuously supplied. We used a travelling random grating to measure the receptive field size (Davis and Naka, 1980). In the turtle experiments two simultaneous recordings were made from luminosity horizontal cells separated by about 0.4 mm. Comparison of the simultaneously recorded receptive field profiles enabled us to identify small (L2-HC) and large (LI-HC) field responses (Simon, 1973; Lam, 1976). Results described here were based on the small field responses. Catfish data were from the horizontal cell soma. In both cases, the horizontal cell bodies receive mainly the red cone inputs (Simon, 1973; Naka, 1969). Experiments were performed at a room temperature of 20°C. Step-evoked responses from the turtle horizontal cells had the characteristic initial peak followed by a plateau phase. The responses were very similar to those seen by other authors (Cervetto and MacNichol, 1972). The stimulus used was whitenoise modulated light with a mean irradiance of Z.O~W/cm’ at the retina [log neutral density filters were used to attenuate this beam to obtain the data for Fig. 2(B)]. The stimulus covered the entire surface of the retina. Electrophysiological recording was conventional. Intracellular responses were tape recorded along with the input signal monitored simultaneously by a United Detector Technology UDT
*Present
address:
X.Y. 10021. U.S.A. I I? Japan.
‘Hunter and ‘Nippon
Horizontal cells
College. 695 Park Ave.. Medical School, Tokyo,
II7
R. k
I3
I
Frequency
CH.APPCLL
!CC
Hz
t’r d
the possibilities of our results havmg been due to seasonal factors or conditions of speclmcns. Over the entire range. the impulse response :ti the cattish horizontal cell to an incremental stimulus has substantially shorter peak response times than that of the turtle. The curves are non-parallel 30 that a simple shift along the lop intensity axis as might be suggested for the difTerencr In the (static) sensitivit;. of the two retinas would not account for the difference. Furthermore. one would expect the maximal eytursion of the response in the turtle to be smaller. IIO: larger, than that of the catfish horizontal cells If only that wx involved. In fact. for a given impulse stimulus. since the amplitude of the response in the turtle horizontal cells is twice that of the cattish [shown h> the PDFs
B
-15mV
Fig. I(A). Power spectra of the two stimulus inputs and of the responses evoked. Data for the turtle experiment are in dashed lines and those for catfish in solid lines. Power (20 decibels per division) of the inputs, plotted as a function of frequency (Hz), is nearly flat up to 70 Hz. (B) Probability density functions (PDFs) for the responses whose power spectra are shown in l(A) above. The ordinates for the two distributions have been scaled so that the peaks of the distributions overlap. Mean of the curves was the average level of hyperpolarization around which modulation was superposed. The two curves were laterally displaced so that their means coincided. The excursion amplitude for the turtle was twice that observed in the catfish.
in Fig. l(B) (Naka et al., 1982). This linearity is consistent with the observations made by Tranchina
ef al. (1981) with the turtle horizontal cells but is in contrast with those made by Baylor and Hodgkin (1973) with the step-evoked receptor response. We note that (1) both kernels had almost identical waveforms as we would expect from the power spectra of Fig. l(A) and (2) there was a fixed delay of 20 msec between catfish and turtle kernels. Comparable data obtained over 4 log units of mean intensity (by using log neutral density filters to attenuate the beam without altering the depth of modulation of the stimulus) is summarized in the graph of Fig. 2(B). Turtle data, in circles, were an average of 7 complete runs whereas catfish data, in triangles, were an average of 6 complete runs. (In the figure legends standard deviations are given.) These data were obtained over a period of I year excluding
E
Fig. 2(A). First order Wiener kernels obtained from analysis of responses to the white noise stimuli. Kernels were normalized: one division on the ordinate is 9 mV/)c W/see for catfish and I7 rnV,p Wisec for turtle. Physiologically these kernels represent the imputse response of the eells superposed on the steady hyperpoiarization. The cattish horizontal cell impulse response (solid line) has a waveform almost identical with that from the turtle (dashed line). The catfish response is faster with a delay of 20 msec between the catfish and turtle kernels. Mean square errors (MSEs) were less than 101; for each. As one would exoect from the PDFs in Fig. I(bi the amplitude of the turtle kernel was twice that of the catfish kernel. (B) Peak response time for turtle and catfish. Peak response times for catfish (triangtes) and turtle (circles) first order kernels are plotted as a function of mean intensity. The incident beams were attenuated using fog neutral density filters in order to obtain the data at additional mean intensities with the same depth of modulation of the stimulus. The impulse response of catfish ceits was consistently faster than that of the turtle over the entire range investigated. The maximal irradiance was 2 PWfcm’. Turtle data was a mean of 7 runs and catfish data was a mean of 6 runs, each run covering a range of 3 log units. Standard deviations (from the brighter to dimmer means) were 1.3. 3.8, 7.5 and 6.1 for turtle and 4.9. 5.2. 5.8 and 12.3 for catfish points.
Kernel
responses
chardcterlze
in Fig. i(B) and scales of the kernals given in Fig. 2(A). legend]. the turtle horizontal cells will have hyperpolarized by almost the same amount as those of the catfish at the time the cattish horizontal cells reach their peak and begin to repoiarize. The turtle cells will go on to reach a peak which is twice as great as that reached by the catfish ceils although this results in prolonging the response. The cattish peak response time curve of Fig. 3(B) is almost identical vvith a plot of the time to half amplitude of the turtle kernels at each intensity. It appears, then, that compared with the turtle, the catfish horizontal cell response latency is signilicantly shorter but the response’s dynamic gain is half that of the turtle response. In summary, our results have demonstrated that turtle horizontal cells had a larger dynamic (incremental) gain than catfish cells but that this gain was concomitant with a longer delay and peak response time. Here we note that the step evoked response from turtle cells had the well documented initial (hyperpolarizing) peak followed by a plateau whereas catfish horizontal cells produced an almost square-looking response. In both retinas the horizontal cells from which the present results were obtained receive direct synaptic input from the receptors. The longer delay of the turtle horizontal cells might have been due to longer delay in the turtle receptors or might have been due to longer transmission delay between the receptor and horizontal cells or a combination of both. Additional experiments are apparently needed to explore further these interesting observations. We have shown in this report that there
119
differences
are subtle but functionally important diRerences between the horizontal cell responses from ditTerent species. Acl;nu~~,lelf~ernenl-Supported partly bq NIH Grants EY00777 and EY-01897. REFEREXES
Baylor
D. A. and Hodgkin A. L. (1973) Detection and resolution of casual stimuli by turtle photoreceptors. J. Phssiof.. Lord. 234. 163-198. Cervetto L. and .MacNichol E. F. Jr (1972) Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Scirvrcr 178. 367-768. Davis G. W. and Naka K.-I. (1980) Spatial organization of catfish retinal neurons. I. Single- and random-bar stimulation J, Newophysiof. 43. 807-83 I. Lam T. D. (1976) Spatial properties of horizontal cell responses in the turtle retina. J. Phy.riof.. Lund. 263. 239-235. Marmarelis P. 2. and Marmarelis V. Z. (1978) rlnu!,~si.s 01‘ Ph~~ioli~#icaf S?:rtetm: Whfte-noi.se ~pp~oij~t~. Plenum, New York. Marmarelis P. Z. and Naka K.-i. (1973) Noniinrar analysis and synthesis of receptive-field responses in the catfish retina. II. One-input white-noise analysis. J. ,Veurophysiof. 36, 634648. Naka K.-l. (1969) Computer assisted analysis of Spotentials. ~j~~~~~. J. 9, 845-859. Naka K.-I., Chan R. Y. and Yasui S. (i97Y) Adaptation in catfish retina. .!. Neurophysiol. 42, 441454. Naka K.-l.. Sakuranaga M. and Chappell R. L. (1982) Wiener analysis of turtle horizontal cells. Blamed. Res. (Suppf.) 3, 131-136. Simon E. J. (1973) Two types of luminosity hortzontal cells in the retina oi the turtle. J. Plr~~io(., Land. 230. 199-21 I. Tranchina I)., Gordon J., Shapley R. and Toyoda J. (1981) Linear information prozssing in the retina: A study of horizontal cell responses. Proc. nn/n. Acnd Sci. U.S.A. 78, 6540-6542.