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The Journal of Neuroscience, May 1, 1998, 18(9):3451-3459
Response to Change Is Facilitated by a Three-Neuron Disinhibitory Pathway in the Tiger Salamander Retina
Botond Roska, Erik Nemeth, and Frank S. Werblin Division of Neurobiology, Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720
ABSTRACT
Top
Abstract
Introduction
Most retinal ganglion cells respond only transiently, for ~150 msec at the onset and termination of a light flash. The responses are transient because it has been shown that bipolar-to-ganglion cell transmission is truncated after 150 msec by a feedback inhibition to bipolar cell terminals. The feedback inhibition itself must be delayed by ~150 msec to allow the initial bipolar-ganglion cell transmission. This study identifies a three-component serial synaptic pathway from glycinergic amacrine cells to GABAergic amacrine cells to bipolar cell terminals as one source of this delay. We used perforated and whole-cell patch-clamp recordings to measure the timing of light responses in amacrine, bipolar, and ganglion cells under control and glycine and GABA receptor-blocked conditions. Our results suggest that, after a light flash, a population of glycinergic amacrine cells responds first, inhibiting a population of GABAergic amacrine cells for ~150 msec. The GABAergic amacrine cells feed back to bipolar terminals, but only after the 150 msec delay, allowing the bipolar terminals to excite ganglion cells for the first 150 msec. Blocking the glycinergic amacrine cell activity with strychnine allows the GABAergic system to become active earlier. GABAergic amacrine cells then inhibit release from bipolar cells earlier. Under these conditions, the ganglion cell response to change would be decreased.
Key words: amacrine cell; glycine; GABA; disinhibition; reciprocal inhibition; retina; patch clamp
INTRODUCTION
A majority of retinal ganglion cells in the salamander retina respond transiently, generating a brief burst of activity at the onset and termination of a light flash. Previous studies suggested that this transient response was mediated by a feedback inhibition from amacrine cells, truncating release from bipolar cell terminals (Dowling and Werblin, 1969
; Burkhardt, 1972
It is well established from analysis of anatomical measurements that amacrine cells form both serial and reciprocal synapses throughout the inner plexiform layer in a variety of vertebrates (Dowling and Boycott, 1966
Previous studies in salamander have identified two main amacrine cell classes, a narrow-field cell with a lateral spread of processes of ~150 µm that contains GABA and a wide-field cell with a lateral spread up to 500 µm that contains glycine. Both cell types appear to have both glycine and GABA receptors. Both cell types make synaptic contact with other amacrine cells, but only GABAergic cells make feedback synaptic contact to bipolar cell terminals (Barnes and Werblin, 1987
We show here that the wide-field amacrine cells respond first, inhibiting the narrow-field amacrine cells. The narrow-field amacrine cells respond only after a delay and make delayed inhibitory synaptic contact with bipolar cell terminals, generating a delayed feedback inhibition. This allows bipolar cells to excite ganglion cells briefly before being inhibited by the delayed feedback.
MATERIALS AND METHODS
Preparation. Experiments were performed on larval tiger salamander slices described by Werblin (1978)
Whole-cell patch-clamp recording. Whole-cell patch-clamp recordings (Hamill et al., 1981
in the control bath solution. The voltage- and current-clamp recordings were performed with an Axopatch 200B patch-clamp amplifier (Axon Instruments, Foster City, CA). The signal was filtered at 1 kHz and digitized at 1 kHz (voltage-clamp mode) or 3 kHz (current-clamp mode) by a 100 kHz Lab Master DMA board (Scientific Solutions, Solon, OH) in a personal computer. The recording software Patchit was developed by George Grant (Grant and Werblin, 1994
12 mV and is corrected by a constant offset during the experiment.
Perforated patch-clamp recording. Nystatin-perforated patch (Horn and Marty, 1988
Bath solution. The control bath solution contained (in mM): 108 NaCl, 2.5 KCl, 2 CaCl2, 1 MgCl2, 5 HEPES, and 10 glucose. The pH was adjusted to 7.8 with NaOH. The blockers were added to the control solution. The concentrations of the blockers were 10 µM strychnine, 100 µM bicuculline, and 100 µM picrotoxin. All drugs were purchased from Sigma (St. Louis, MO) unless otherwise indicated.
The solutions were changed by a gravity-driven perfusion setup with a 3-4 ml/min flow rate at room temperature.
Electrode solution. The composition of the patch electrode solution (in mM) was the following: 101 Kgluconate, 8.5 KCl, 0.0078 CaCl2, 1 MgCl2, 0.1 BAPTAK4, 10 HEPES, 4 ATPNa2, and 0.5 GTPNa3. The pH was adjusted to 7.4 with KOH. The calculated ECl was
Light stimulus. We used a red light-emitting diode set to its maximum intensity to stimulate the retinal slice and sufficient to elicit a maximal response from each cell type studied here.
Cell identification. Cells were identified by their light response and morphology. To reveal morphology, we patched clamped the measured cell after the experiments with another patch electrode containing 1% Lucifer yellow (Aldrich, Milwaukee, WI) attached to a PC 501-A patch-clamp amplifier (Warner Instrument, Hamden, CT). Cells were viewed using a Nikon mercury fluorescent epi-illuminator with an XF15 filter set (Omega Optical, Brattleboro, VT).
Classification of amacrine cells as ON-OFF or ON amacrine cells. We classified an amacrine cell as ON-OFF if the cell, voltage clamped to
RESULTS
Yang et al. (1991)
Narrow-field amacrine cells are inhibited via both glycine and GABAA receptors
Figure 1A shows the voltage response typical of 13 of 18 narrow-field cells that generated a train of spikes at the onset and one or two spikes at the termination of the light step. The responses of the same cell under voltage clamp are shown in Figure 1B. The currents reversed at negative potentials near
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Figure 1. The light response, synaptic currents, and morphology of a narrow-field amacrine cell. A, The ON-OFF voltage response to a full-field red light step stimulus. B, Current responses of the same cell to the same stimulus voltage clamped to the potentials indicated at the right of each trace. The light-evoked current reversed near
We used the light responses when the cell was voltage clamped to 0 mV to isolate the inhibitory currents so that we could measure the dynamics of these responses. Subtracting the response in strychnine from the control response revealed the magnitude and dynamics of glycinergic inhibition to this cell (ON time to peak, 121 ± 36 msec; peak magnitude, 94 ± 34 pA; n = 9; OFF time to peak, 138 ± 82 msec; peak magnitude, 217 ± 140 pA; n = 9). Subtracting the response in the presence of bicuculline from the control response revealed the dynamics of the GABAergic inhibition via GABAA receptors (ON time to peak, 166 ± 79 msec; peak magnitude, 37 ± 44 pA; n = 4; OFF time to peak, 135 ± 50 msec; peak magnitude, 28 ± 35 pA; n = 4).
The effect of the transient glycinergic inhibition on the voltage response of a narrow-field amacrine cell is shown in Figure 2. The transient glycinergic inhibition (Fig. 2A) seems to cause an early suppression of activity of the narrow-field amacrine cell. The timing of the delay in the onset of spiking (Fig. 2C, dark bar) matched the timing of the glycinergic inhibitory current (Fig. 2A). Blocking glycine receptors with strychnine eliminated both the transient inhibitory current (Fig. 2B) and the delay of spiking (Fig. 2D).
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Figure 2. Glycinergic inhibition causes a delay in the light-evoked activity of the narrow-field amacrine cells. A, A transient inhibitory current at light ON is shown. B, The inhibition is glycinergic and was blocked by strychnine. C, The normal light response of the cell was delayed by ~150 msec at light ON. D, The delay was eliminated by blocking glycinergic receptors with strychnine. The duration of the inhibitory current (A) corresponds with the timing of the delay (C) as designated by the dark vertical bars.
The light response under current clamp measured in one of the other five narrow-field amacrine cells studied is shown in Figure 3A. These cells responded with a transient burst of spikes only at light ON that was not sustained throughout the duration of the light step. The responses of the same cell under voltage clamp are shown in Figure 3B. The currents were generated only at light ON but otherwise were similar to those measured in the ON-OFF cell shown in Figure 2; they reversed at negative potentials, near
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Figure 3. The light response, synaptic currents, and morphology of the narrow-field ON amacrine cells. A, The light response to a full-field red light stimulus. This cell type responds only at light ON. B, The current responses of the same cell to the same stimulus voltage clamped to the potentials indicated at the right of each trace. The inhibitory currents appear only at light ON. The light-evoked current reversed near
Activity in wide-field amacrine cells is truncated by GABAergic inhibition
A typical light response of a wide-field amacrine cell under current clamp is shown in Figure 4A. These cells generate a single spike at light ON and another single spike at light OFF (Werblin, 1977
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Figure 4. The light response and morphology of a wide-field amacrine cell. A, The light response of a wide-field amacrine cell that characteristically fires only one spike at light ON and OFF followed by a slow decay in response. B, Stylized sketch of the cell filled with Lucifer yellow. Processes ramify in both sublaminae A and B (Sl.A and Sl.B) and spread laterally over ~400 µm.
In three out of nine wide-field cells studied, no glycinergic inhibition could be measured. After perfusion with strychnine, the inhibitory response remained unchanged or increased slightly (compare Fig. 5A and B). Figure 5C shows that bath application of bicuculline together with strychnine blocked the inhibitory outward current at 0 mV, suggesting that the primary inhibitory input to these wide-field cells arrives via GABAA receptors. The increased GABAergic inhibition might be caused by the increased activity of GABAergic narrow-field amacrine cells when glycinergic inhibition to them was blocked. The remaining inward current is present probably because the membrane was not clamped to precisely the reversal potential for the excitatory inputs.
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Figure 5. The effects of strychnine and bicuculline on the outward currents in wide-field amacrine cells. A, The current response of a wide-field amacrine cell voltage clamped to 0 mV and showing outward currents at light ON and OFF is shown. B, Strychnine had minor effects on the magnitude of the currents in the same wide-field amacrine cell. C, The outward currents were blocked by bicuculline, suggesting that they arrive at these cells via GABAA receptors. The remaining inward current is probably attributable to the fact that the cell was not clamped at the exact reversal potential for the excitatory currents.
The GABAergic input to the wide-field glycinergic amacrine cells seems to be responsible for this characteristic single-spike activity. Figure 6A shows the outward current in the presence of strychnine measured in a wide-field amacrine cell held at 0 mV. Figure 6B shows that this outward current was eliminated with the addition of bicuculline, thought to block GABAA receptors.
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Figure 6. GABAergic inhibition truncates spiking in wide-field amacrine cells. A, When voltage clamped to 0 mV in the presence of strychnine, wide-field amacrine cells receive a strong inhibitory current. B, Bicuculline blocks this inhibitory current. C, The typical light response of the wide-field amacrine cell consisting of a single spike persists in strychnine. D, The addition of bicuculline, which eliminates the GABAA-mediated inhibition, makes the light response more sustained. Light now elicited a train of spikes. The delayed GABAergic inhibition (A) constrains the cell to fire only one spike at light ON (C). The dark vertical bars show the time interval of ~150 msec for GABAergic inhibition.
When the GABAergic inhibition was blocked, the normal single-spike response of this cell class (Fig. 6C) was extended to a train of spikes with decreasing amplitude (Fig. 6D). But even in the absence of the glycine-mediated delay (measured in the presence of strychnine), wide-field amacrine cells still generated only a single spike. This suggests that the GABAergic inhibitory signal is inherently delayed with respect to the excitatory input, even in the absence of a glycinergic input (Fig. 6C).
In six out of nine wide-field amacrine cells tested, we measured glycinergic as well as GABAergic inhibition, but blocking the glycinergic inhibition did not significantly change the form of the voltage response. The glycinergic input was apparently small enough that the cell membrane could still reach threshold to initiate the single-spike response. The blockage of GABAA receptors had effects similar to those measured in other wide-field cells described in Figure 6. The function of the glycinergic inhibition to these cells is unclear.
GABAC inhibition at ON bipolar cells was increased as glycine and GABAA receptors were blocked
Viewed from the perspective of the bipolar cell terminal, the inhibitory pathway comprises three neurons in a serial synaptic chain. One possible pathway includes wide-field amacrine to narrow-field amacrine to bipolar terminal. When recording from bipolar cells, we encountered measurements that may reflect the serial inhibitory action of this neuronal chain. We found an increase in inhibition at bipolar cells that was brought about by the bath application of inhibitory blockers.
We isolated the inhibitory currents by voltage clamping bipolar cells to 0 mV. Figure 7A shows these inhibitory outward currents at light ON and OFF under control conditions in an ON bipolar cell. The inhibitory currents were augmented in the presence of strychnine in six out of nine cells (Fig. 7B). The currents were further augmented by perfusion with strychnine plus bicuculline (Fig. 7C). However, the currents were completely blocked in the presence of strychnine, bicuculline, and picrotoxin (Fig. 7D). This suggests that the final synapse in this disinhibitory chain lies at the GABAC receptors at the bipolar cell synaptic terminals (Feigenspan et al., 1993
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Figure 7. The inhibition recorded in an ON bipolar cell is enhanced in the presence of strychnine and further enhanced by bicuculline. A, ON bipolar cells normally generate small inhibitory currents when voltage clamped to 0 mV at both light ON and OFF. B, The inhibition was enhanced in the presence of strychnine. C, The addition of bicuculline further enhanced the inhibitory currents at both light ON and OFF. D, The inhibition was blocked by the addition of picrotoxin, suggesting that the inhibition is mediated via GABAC receptors.
Truncation of the bipolar cell response is delayed by a glycinergic signal
Dong and Werblin (1997)
Application of strychnine had two effects on cells presynaptic to the ganglion cells. Strychnine decreased the delay in GABAergic amacrine cell activity (Fig. 2D) and increased the outward currents measured in bipolar cells (Fig. 7C). When we measured from ganglion cells, the application of strychnine should cause excitation to occur later (because early release is blocked) or to be diminished (because inhibition is increased at bipolar cells). We found evidence of both of these effects in recordings from ganglion cells held at
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Figure 8. The strychnine-mediated changes in excitatory currents measured in two ganglion cells. Cells were clamped to
DISCUSSION
Numerous authors have proposed that transient responses in ganglion cells are mediated by feedback inhibition at bipolar terminals from amacrine cells (Dowling, 1968
Timing of the two components of the reciprocal relation
Our measurements suggest that reciprocal inhibition between the two main amacrine cell classes, the narrow- and wide-field cells (Yang et al., 1991
A complimentary scenario exists in the wide-field glycinergic amacrine cells shown in Figure 6. These cells receive a GABAergic input via GABAA receptors as shown by the blockade of this inhibition with bicuculline in Figure 6B. The delayed activity of the narrow-field cells seems to truncate spike activity in these cells, because when the GABAergic inhibition is blocked, the cells, which normally generate only a single spike (Fig. 6C), continue to spike throughout the stimulus duration (Fig. 6D). The "control" traces of Figure 6 were measured in the presence of strychnine.
Figure 2 shows that strychnine removed a significant delay in the GABAergic amacrine cell response. Figure 6 shows that even with this delay removed, the glycinergic amacrine cells still respond with an initial single spike. This comparison suggests that there is an inherent delay in the GABAergic neurons, even without the influence of the glycinergic inhibition shown in Figure 2.
An important consequence of this interaction is that the activity of the narrow-field GABAergic amacrine cells is actively delayed by an early inhibition from the wide-field amacrine cells (Fig. 2C). The narrow-field amacrine cells inhibit the bipolar cells, so the delayed inhibition of the narrow-field cells allows an early release from the bipolar terminals. This is manifest as an early excitation in ganglion cells (Fig. 8A) and may be a crucial component for the generation of a transient response.
Possible mechanisms underlying the timing of reciprocal inhibition in amacrine cells
The relative timing of the activity of the two classes of amacrine cells seems to be dominated at early times by the robust spiking mechanism in the wide-field amacrine cell. Wide-field amacrine cells show a very low threshold for spiking (Werblin, 1977
Possible circuitry for disinhibition at bipolar cells
The results of Figure 7, showing that the inhibitory input to the bipolar cells is enhanced in the presence of strychnine and bicuculline, suggest the presence of at least two disinhibitory pathways that are expressed in the GABAC-mediated inhibition at bipolar cells. One involves wide-field amacrine cells acting via a glycinergic pathway that is blocked by strychnine (Fig. 7B). The other involves a class of GABAergic amacrine cells acting via a GABAA pathway (Fig. 7C). A possible circuitry underlying these findings is outlined in Figure 9.
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Figure 9. A proposed circuitry and time courses of cellular responses for serial synaptic connections mediating the delayed inhibition at bipolar cell terminals. Each cell icon represents a local population of cells. After a light flash (bottom stepped horizontal lines), wide-field amacrine cells (Wf) are active first (A). The wide-field cells inhibit narrow-field amacrine cells (Nf), delaying their activity (C). This allows bipolar cells (Bip) to excite ganglion cells (Gang) at early times (E). In the presence of strychnine, the glycinergic input to the narrow-field amacrine cell is lost (B). This allows the narrow-field cells to fire sooner (D), delaying the activity in the ganglion cells (F). The dotted line in F was copied from E to show the difference in timing. The dark vertical bars indicate the time interval during which the glycine-mediated delay is present.
A possibility for both wide-field and narrow-field glycinergic amacrine cell types
In their original classifications, Yang et al. (1991)
Yang et al. (1991)
Explanation for the discrepancy between our results and those of Yang et al. (1991)
Yang et al. (1991)
The effects of reciprocal inhibition and disinhibition on ganglion cells
Zhang et al. (1997)
FOOTNOTES Received Nov. 19, 1997; revised Jan. 29, 1998; accepted Feb. 18, 1998.
This work was supported by National Institutes of Health Grant NEI-00561. B.R. is supported by a Fulbright Fellowship.
Correspondence should be addressed to Dr. Frank Werblin, 145 Life Sciences Addition, Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, CA 94720.
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Copyright © 1998 Society for Neuroscience 0270-6474/98/1893451-09$05.00/0
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