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The Journal of Neuroscience, September 1, 2002, 22(17):7712-7720
Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina
W. Rowland Taylor1 and David I. Vaney2 1 John Curtin School of Medical Research and Centre for Visual Sciences, Australian National University, Canberra, 2601 ACT, Australia, and 2 Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, The University of Queensland, Brisbane, QLD 4072, Australia
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
The synaptic conductance of the On-Off direction-selective ganglion cells was measured during visual stimulation to determine whether the direction selectivity is a property of the circuitry presynaptic to the ganglion cells or is generated by postsynaptic interaction of excitatory and inhibitory inputs. Three synaptic asymmetries were identified that contribute to the generation of direction-selective responses: (1) a presynaptic mechanism producing stronger excitation in the preferred direction, (2) a presynaptic mechanism producing stronger inhibition in the opposite direction, and (3) postsynaptic interaction of excitation with spatially offset inhibition. Although the on- and off-responses showed the same directional tuning, the off-response was generated by all three mechanisms, whereas the on-response was generated primarily by the two presynaptic mechanisms. The results indicate that, within a single neuron, different strategies are used within distinct dendritic arbors to accomplish the same neural computation.
Key words: direction selectivity; ganglion cells; synaptic conductance; inhibition; excitation; dendritic integration; on- and off-pathways; rabbit retina
INTRODUCTION
The direction-selective ganglion cells (DSGCs) in the rabbit retina are a model system for investigating neural computation (Vaney et al., 2001
). These cells respond strongly to an image moving in a preferred direction but only weakly to an image moving in the opposite "null" direction. The foundation for understanding the cellular mechanisms of direction selectivity in vertebrates was laid by Barlow and Levick (1965)
Torre and Poggio (1978)
Such a postsynaptic model contrasts with a presynaptic model in which the inputs to the DSGC are themselves directionally selective. There are two basic versions of the presynaptic model: (1) the excitatory inputs to the DSGC are larger in the preferred direction, and (2) the inhibitory inputs to the DSGC are larger in the null direction. These two versions could also coexist, with both the excitation and inhibition being directional. Moreover, presynaptic and postsynaptic mechanisms are not mutually exclusive and could conceivably be combined within a single ganglion cell.
A study of rabbit DSGCs by Taylor et al. (2000)
Thus, the findings and conclusions from the turtle study are almost diametrically opposed to those from the rabbit study, leading us to undertake a similar conductance analysis of the light-evoked responses of DSGCs in the rabbit retina.
MATERIALS AND METHODS
Animals and patch recording. The experiments comply with the Australian Capital Territory Animal Welfare Act (1992) and were approved by the Animal Experimentation Ethics Committee of the Australian National University. Dark-adapted, New Zealand White rabbits were surgically anesthetized, and the right eye was removed under dim-red illumination. The animal was then killed by anesthetic overdose. All subsequent manipulations were performed under infrared illumination. The front of the eye was removed, the eyecup was transected just above the visual streak, and the dorsal piece was discarded.
The retina was dissected from the sclera, and a 10 × 10 mm section of central retina was adhered, photoreceptor-side down, to a coverslip coated with CellTak (BD Sciences, Bedford, MA). The whole-mount retina preparation was placed in a recording chamber (~0.5 ml volume) and perfused continually (~2 ml/min) with oxygenated bicarbonate-buffered Ames medium, pH 7.4, at 33-37°C. Patch electrodes were pulled from borosilicate glass to have a final resistance of 4-8 M
.
For extracellular recording, the electrodes were filled with the Ames medium. For intracellular recording, the electrodes were filled with the following electrolytes: 110 mM Cs-gluconate or CsCl, 10 mM NaCl, 5 mM Na-HEPES, 1 mM Cs-EGTA, 1 mM Na-ATP, 0.1 mM Na-GTP, and 10 mM QX-314 (Sigma-Aldrich). Cesium was used in place of potassium to block voltage-gated potassium currents and thereby improve the quality of the voltage clamp at positive potentials. The QX-314 was included to block voltage-dependent sodium channels and abolished all spiking activity within 1-2 min of establishing the whole-cell configuration. The liquid junction potential of 10 mV was subtracted from all voltages when the intracellular solution contained Cs-gluconate.
Ganglion cells with a medium-large soma and a crescent-shaped nucleus were targeted as potential DSGCs (Vaney, 1994
Light stimuli. Light stimuli were generated on a Barco Systems monitor (refresh rate, 72 Hz) and focused onto the photoreceptor outer segments through a 40 × [numerical aperture (NA) 0.75] or 20 × (NA 0.35) Olympus water-immersion objective. The stimulus contrast, defined as C = (Lmax
Lmin)/(Lmax + Lmin), was set between 0.3 and 1.0. The standard moving stimulus comprised a light or dark bar, moving along its long axis at 800-1200 µm/sec on the retina. All light stimuli were centered with respect to the tip of the recording electrode and thus also with the soma of the ganglion cell. Relative timing of the responses in the preferred and null directions is made directly from the recorded responses without correction for possible spatial offset of the receptive fields. Justification for this is presented in the results. The width of the bar was 250 µm, and its length was set to achieve good temporal separation of the leading- and trailing-edge responses. These responses are clear in the Figures, but more often a distinction will be made between the on-response and the off-response. Because the stimulus could be either a light or dark bar, the leading-edge response could be either an on-response or an off-response.
Conductance analysis. Conductance analysis methods were similar to those described by Borg-Graham (2001)
where gT(t) = ge(t) + gi(t), and Vr(t) is the observed reversal potential. Thus, Vr(t) is the weighted sum of Ve and Vi such that:
(1)
(2) Inspection of Equation 2 reveals that if the time courses of gi and ge are equal (can be superimposed under scalar multiplication), then Vr(t) = constant (see Fig. 2). Equation 2 can be rearranged to separate the excitatory and inhibitory components from gT(t) and Vr(t), where:
(3)
(4) Separation of the components required assigning values to the reversal potentials for excitation and inhibition, Ve and Vi, in Equations 3 and 4. Application of these equations to the biophysical system studied here places constraints on Ve and Vi. First, because of the ionic selectivity of the channels and the ionic gradients in the neurons, Vi < Ve. This will also be true when the high-chloride intracellular solutions are used, because it is unlikely that the chloride concentration within the dendrites will attain the chloride concentration in the recording electrode, because of chloride extrusion across the dendritic membranes (Vardi et al., 2000
0, which means that Vi
Vr
Errors in the assignment of the reversal potentials will result in quantitative errors in the estimates of the conductance ratios. The cell illustrated in Figure 2 provides a convenient example. If we were to set Vi to
0. Because Vr approaches 0 mV in the preferred direction, indicating ge > 0, an almost infinite preferred-null conductance ratio for ge would be predicted. Therefore, the constraint that Vi not exceed
The synaptic conductance and reversal potential were evaluated as follows. Synaptic currents were elicited by moving the stimulus in the preferred and null directions at a series of holding potentials starting at
Because thousands of I-V relations were generated, it was not practical to fit and inspect the I-V manually at each time point. Therefore, an automated routine was implemented using Igor Pro to perform linear regression on the I-V relations (Wavemetrics, Lake Oswego, OR). In some cells, the I-V relations at the most negative and most positive voltages were sublinear, tending to bend toward the voltage axis. At negative potentials, the nonlinearity could reflect activation of NMDA receptors, which are known to be expressed in these neurons (Kittila and Massey, 1997
A direction-selectivity index, D, was calculated as a measure of the directional tuning. Extracellular action potentials were recorded in each of 8 or 12 stimulus directions, equally spanning 360° at 45 or 30° intervals. D was defined for the action potential discharges as:
where
(5) i are vectors pointing in the direction of the stimulus and having length, ri, equal to the number of spikes recorded during that stimulus. D can range from 0, when the responses are equal in all stimulus directions, to 1, when a response is obtained only for a single stimulus direction. Thus, values for D approaching 1 indicate asymmetric responses over a small range of angles and therefore sharper directional tuning.
RESULTS
Directional tuning
The preferred-null axis of each cell was established from extracellular recordings. A stimulus bar was swept across the receptive field in 12 directions, spaced at 30° intervals (Fig. 1). The stimulus direction that generated the most action potentials was designated as the preferred direction, and the opposite direction was designated as the null direction. This preferred-null axis was used for all further stimuli during subsequent patch-clamp recordings. The preferred direction was calculated more precisely, during later analysis, from the vector sum of the leading- and trailing-edge spikes (Fig. 1, arrow). In a sample of 10 cells, the average absolute difference between the estimated preferred-null axis and the calculated axis was 12 ± 8°, with the largest difference being 28°. The calculated preferred directions for the on- and off-responses agreed very closely, differing by only 0.3 ± 11° in a group of 11 cells. Directional tuning, evaluated as defined by Equation 5 in Materials and Methods, was the same for the on- and off-responses (Table 1).
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Figure 1. Determination of the preferred-null axis. The distance from the origin represents the total number of spikes produced by the leading edge ( ) or trailing edge (
) of a single stimulus. The surrounding traces show the extracellular responses for the corresponding directions. The first burst of spikes, produced by the leading edge of the stimulus bar, is the off-response, because the moving bar was darker than the background (0.7 contrast). The second burst of spikes, produced by the trailing edge, is the on-response. The preferred directions for the on- and off-responses, calculated from the vector sum of the data points, were indistinguishable in this cell, and therefore they are marked by a single arrow, the length of which has been truncated; the lengths of the vector sums were 117 spikes for the on-responses and 120 spikes for the off-responses.
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Table 1. Directional index, conductance ratios, timing differences, and spatial offsets Synaptic current-voltage relations
After the DSGC was patched, the membrane potential was stepped to a range of levels, and the visual stimulus was swept in opposite directions along the preferred-null axis. At negative potentials, the peak inward currents in the preferred and null directions were coincident both for the on- and off-responses, suggesting that the receptive field of the DSGC was well centered with respect to the stimulus (Fig. 2A,B). Therefore, comparisons of response timings in preferred and null directions are made directly from the records.
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Figure 2. Analysis of the membrane conductance during motion along the preferred-null axis for a single stimulus. Blue data represent preferred direction; red data represent null direction. A, B, Synaptic currents elicited by a bright bar moving in the preferred and null directions at a series of holding potentials starting at
The sets of current records for the preferred and null directions (Fig. 2A,B) show systematic changes in the time course of the responses as a function of the holding potential, reflecting the changing balance of excitation and inhibition that occurs as the stimulus sweeps across the receptive field. In particular, at positive holding potentials, where the inhibitory inputs are more evident, the pronounced differences in the current wave-forms for preferred and null directions support the hypothesis that postsynaptic inhibition is important for generating direction selectivity (Taylor et al., 2000
A quantitative analysis of these responses was performed by generating I-V relations of the net light-evoked current every 10 msec for the duration of the visual responses. The I-V relations were essentially linear over much of the voltage range (Fig. 2E), and the conductance was estimated by fitting a straight line to each I-V plot. The fitted lines provided two parameters at each time point: the intercept, giving an estimate of the synaptic reversal potential Vr (Eq. 1; Fig. 2C,F,G), and the slope, giving the size of the light-evoked conductance gT (Fig. 2D,H).
Synaptic reversal potential
The trajectory of the synaptic reversal potential was similar in every DSGC. In the preferred direction, Vr ramped up rapidly toward 0 mV during the early phase of the response, to both the leading edge (on-response) and the trailing edge (off-response) of a positive-contrast stimulus (Fig. 2C, blue line). Vr then ramped down during the late phase of the response, typically ending around
In the null direction, Vr generally remained negative, consistent with the dearth of spikes in the extracellular recordings. During the late phase of the off-response, however, Vr consistently ramped toward more positive values, producing a crossover in the reversal potential trajectories. When a positive-contrast stimulus was used, the crossover occurred during the late phase of the trailing-edge response (Fig. 2C,F, X arrow). When a negative-contrast stimulus was used, the crossover occurred during the late phase of the leading-edge response (Fig. 2G, X arrow). The presence or absence of the crossover was robust enough to allow the sign of the contrast edge to be reliably determined by inspection of the Vr records. Such crossover was never observed in the reversal potential trajectories of the on-response, which superimposed during the late phase of the response, indicating that the synaptic currents were not direction selective at these times. These distinct characteristics suggest that there are basic differences in the synaptic mechanisms underlying direction selectivity for the on- and off-responses.
Synaptic conductance
The peak conductance was larger in the null direction than the preferred direction (Fig. 2D,H). This would be compatible with a presynaptic model of direction selectivity in which inhibition was larger in the null direction, with no change in the time course of the inputs. However, a greater peak conductance in the null direction would also be compatible with a postsynaptic model in which the closer temporal correlation of inhibition and excitation in the null direction results in greater summation of the inhibitory and excitatory conductances, with no change in their relative magnitudes.
The off-response may satisfy the latter possibility. Although the peak off-conductance was smaller in the preferred direction, the waveform was consistently broader (Fig. 2D,H, blue line). Thus it is possible that the same total conductance is activated, but with differing temporal dispersion. In contrast, the on-response appeared to have a very similar time course in the preferred and null directions, more in line with a presynaptic mechanism. The reversal potential trajectories support this interpretation. During the on-response, the reversal potential in the null direction was essentially constant, indicating that excitation and inhibition had very similar time courses (Eq. 2). During the off-response, the reversal potential in the null direction changed continuously, consistent with different spatiotemporal characteristics for the two inputs, as expected for a postsynaptic mechanism.
For a purely postsynaptic model, the total synaptic conductance should be equal in the preferred and null directions, whereas for presynaptic mechanisms, there should be an imbalance. We examined this quantitatively by integrating the conductance records in the two directions. When the preferred GT is plotted against the null GT (Fig. 3), many of the points lie below the unity line, indicating that the integrated conductance was slightly larger in the null direction, averaging 118 ± 23% for 28 DSGCs. Although the difference was small and not shown by some cells, it suggested that there might be presynaptic components to the directional mechanism.
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Figure 3. Integrated conductance. Each point shows a single measurement of the total integrated conductance, GT. The solid symbols show averages of one to three determinations in the 16 cells that were analyzed further. The open symbols show the average of one to three measurements in 12 additional cells.
Excitatory and inhibitory components
To identify whether the asymmetry lies in the excitatory or inhibitory inputs to the ganglion cells, we resolved their separate contributions to the conductance records. Similar to previous electrophysiological studies, we found that the on-response of a DSGC could be quite different in size from the off-response, with the off-responses tending to be larger. To make a meaningful comparison between the on- and off-responses, cells with markedly different responses were excluded from the analysis, leaving a subset of 16 cells with broadly comparable responses (Fig. 3,
To separate the conductance records into excitatory and inhibitory components (Eq. 3 and 4), we made the following assumptions (see Materials and Methods). (1) The DSGC is isopotential; theoretical results from Koch et al. (1990)
The calculated excitatory and inhibitory components provide a rationale to account for the time-dependence of Vr and gT. The qualitative features described here were similar for all cells, although there were marked quantitative differences from cell to cell. The peak amplitude of the excitatory conductance, ge, tended to be larger in the preferred direction, but the overall time course was independent of direction for both the on- and off-responses (Fig. 4A,E). By contrast, the time course of the inhibitory conductance, gi, differed dramatically in the preferred and null directions (Fig. 4B,F).
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Figure 4. Separation of gT into ge and gi. Each trace is the response to a single stimulus. Comparison of the time course of ge (A, E) and gi (B, F) for positive (A, B) and negative (E, F) contrast stimuli. C, D, G, H, The same records replotted to compare preferred- and null-direction responses. The solid lines under the records delineate the intervals used to calculate the direction-selective integrals in Figure 5.
For the off-response, the inhibition in the preferred direction was significantly delayed compared with the null direction, consistent with an asymmetric spatial offset (Fig. 4B,F). For the on-response, a distinction must be made between positive- and negative-contrast stimuli. During negative-contrast stimuli, the inhibition was smaller in the preferred direction but its time course was unchanged, suggesting that presynaptic mechanisms control this input (Fig. 4B). During positive-contrast stimuli, inhibition comprised an early transient phase (Fig. 4F, delineated by the solid line beneath the trace) followed by a sustained phase (Fig. 4F, delineated by the broken line beneath the trace). The magnitude of the early phase was strongly modulated in opposite directions, also consistent with presynaptic direction-selective mechanisms. The late phase of the on-response was nondirectional and superimposed for opposite-direction stimuli. Moreover, synaptic currents active during this late phase did not generate spikes in either direction (Fig. 2F). In contrast, a sustained phase was not present during on-responses elicited during negative-contrast stimuli (Fig. 4B), and it was clear during such responses that, unlike the off-responses, the inhibition is not delayed in the preferred direction. Although it is more difficult to discern during positive-contrast stimuli, the on-responses appeared to lack any inhibitory delay in the preferred direction because, as noted above, the late phase of the on-response was nondirectional (Fig. 4F).
The reversal potential trajectories can be understood in terms of the relative trajectories of the excitatory and inhibitory conductances in each direction. In the preferred direction, excitation dominated because the inhibition was either reduced (on-response) or delayed (off-response) (Fig. 4C,G). In the null direction, Vr was essentially constant during the on-response because the excitation and inhibition had similar time courses (Fig. 4D,H). By contrast, Vr tended to increase during the off-response, leading to the characteristic crossover of the Vr trajectories. The crossover resulted from a fall in the ratio of inhibition to excitation late in the response, attributable to an earlier onset and a narrowing of the inhibitory component. In summary, on-responses appeared to be dominated by a directional inhibitory input, whereas off-responses displayed both a directional inhibitory input and a change in temporal correlation as expected for a postsynaptic mechanism.
The inhibition during the on-responses was invariably larger in the null direction, but it is not clear whether other factors contribute to the imbalance in the total conductance shown in Figure 3. Therefore, we integrated the two conductance components, ge and gi, separately for the on- and off-responses. The integrals for the on-responses during positive-contrast stimuli were calculated over the transient phase (see above), delineated by the solid lines beneath the records in Figure 4F, thereby avoiding the sustained nondirectional inhibition active late in the on-response. Inclusion of this nondirectional component during the analysis only reduced the estimated asymmetry of the on-inhibition.
The excitatory component was larger in the preferred direction (Fig. 5A), and on average, this presynaptic asymmetry was similar for the on- and off-responses (Table 1). Similarly, the inhibitory component was consistently larger in the null direction (Fig. 5B). These differences are illustrated more clearly when the preferred/null Ge ratio is plotted against the null/preferred Gi ratio (Fig. 5C). For a purely postsynaptic scheme, the points should cluster around the intersection of the unity lines. For the great majority of points, both the Ge ratio and the Gi ratio were greater than unity, indicating that the cells received both directional excitation and directional inhibition, consistent with their preferred direction. The off-responses clustered nearer the intersection than the on-responses, indicating that the presynaptic mechanisms were more potent for the on-responses. The mean values of the Ge and Gi ratios for the on- and off-responses are shown in Table 1, which also shows the preferred-null ratio of the total directional conductance, GD, defined as the sum of Ge and Gi evaluated over the "On" and "Off" intervals delineated in Figure 4.
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Figure 5. Integrals of the conductance components for the on-response (A,
For the off-responses, the directional excitation and directional inhibition were of equal magnitude, and thus the total off-conductance was balanced for the preferred and null directions. For the on-responses, directional inhibition tended to be stronger, and thus the total on-conductance was greater in the null direction. The imbalance observed in Figure 3 for the integrated conductance can be attributed, therefore, mainly to the on-response, diluted by the larger off-response, and by inclusion of the nondirectional conductance active during the late phase of the on-response. The broad range of ratios in Figure 5C is noteworthy, indicating that the cells can be direction selective when they receive nondirectional excitation or nondirectional inhibition.
The extent of the spatial offset of the inhibition was estimated from the timing differences of the inhibitory peaks. The calculations assume that the receptive field is centered with respect to the stimulus (which is aligned to the soma) and that the synaptic delays are the same in the null and preferred directions. Consistent with this assumption, the excitatory conductance peaks were coincident in the preferred and null directions (Fig. 4A,E). The absolute peak-conductance time, relative to the start of a stimulus trial, was measured for excitation and inhibition in the preferred and null directions. The difference, dT, preferred minus null was converted into an equivalent spatial offset; for a stimulus speed of
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Figure 6. The off-inhibitory conductance is offset in the null direction. The symbols show the inferred spatial offset, dX, calculated from the shift in the peak-conductance time observed for preferred- and null-direction motion. A positive spatial offset means that the conductance was delayed during preferred-direction motion relative to null-direction motion.
High chloride
Previously, we showed that the inhibition acts directly on the dendrites of the DSGC, and we argued that the direction selectivity is generated postsynaptically (Taylor et al., 2000
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Figure 7. Effect of high intracellular chloride. A, B, Records in response to preferred (blue) and null (red) stimuli at the commencement of the whole-cell recording. C, D, Similar data obtained 7.5 min later. The shift in Vi is evident, but the overall time course and magnitude of the conductances are unchanged.
DISCUSSION
Locus of direction selectivity
The results reported here indicate that direction selectivity is generated by the combination of three distinct synaptic asymmetries: (1) a presynaptic mechanism producing stronger excitation in the preferred direction, (2) a presynaptic mechanism producing stronger inhibition in the null direction, and (3) postsynaptic interaction of the excitation with spatially offset inhibition. The three mechanisms were not uniformly expressed by the on- and off-responses, although the extracellularly recorded responses were very similar. The on-responses appeared to rely on presynaptic mechanisms. The off-responses were more consistent with a mix of presynaptic and postsynaptic mechanisms.
For both the on- and off-responses, the precise mix of presynaptic and postsynaptic mechanisms was quite variable, and in some cells one or another of the presynaptic components was absent (points close to the unity lines in Fig. 5). This variability raises the possibility that DSGCs are programmed to generate a specific functional phenotype during development but that there is considerable latitude in the eventual mix of synaptic mechanisms used to achieve this goal. The large variability in the contribution from each of the three mechanisms, both among different cells and between the on- and off-responses, suggests that no single mechanism is essential for the generation of direction selectivity. Moreover, the mechanistic variability argues against the idea that different mechanisms are required to process different types of visual stimuli (Grzywacz et al., 1998
A postsynaptic mechanism reliant on shunting inhibition requires that the synapses be electrotonically remote from the soma for direction selectivity to be generated locally within the dendritic tree (Torre and Poggio, 1978
The conductance analysis revealed that both the excitatory and inhibitory inputs to DSGCs may be tuned directionally and that the response bias is consistent with the preferred direction of the cells. In an earlier study we argued for a simpler scheme involving only postsynaptic mechanisms (Taylor et al., 2000
Errors in conductance estimates in a non-isopotential neuron
To separate the conductance records into excitatory and inhibitory components, we assumed that the DSGCs were isopotential (Anderson et al., 2000
Koch et al. (1990)
Separation of the conductance into excitatory and inhibitory components also required estimates for the reversal potentials of the two inputs. These were not measured directly and therefore were set to reasonable values: 0 mV for excitation and
The estimation of the presynaptic components relies on the ratio of conductances measured in the preferred versus null directions. Because the total light-evoked conductance was essentially constant in the preferred and null directions (Fig. 3), the conductance errors will be independent of stimulus direction. The conductance errors for the off-responses, however, are complicated by the delay in the inhibitory conductance. The temporal offset of inhibition relative to excitation in the preferred direction will tend to reduce the conductance errors of both inputs, whereas the temporal correlation of the inputs in the null direction will tend to increase the errors. Thus, the excitatory ratio will tend to be overestimated, and the inhibitory ratio will tend to be underestimated. Without quantitative modeling, it is not possible to say how large these errors in estimation might be, but they are probably not large, because the observed conductance ratios were not correlated with the magnitude of the total conductance.
Implications for synaptic circuitry
Our results indicate that direction selectivity for both on- and off-responses is generated to some extent by a push-pull mechanism, where complementary changes in excitation and inhibition drive the cell to a greater or lesser degree with only small changes in overall membrane conductance (Watanabe and Murakami, 1984
Many of the neuronal models of direction selectivity that have been put forward invoke a key role for starburst cells, which are two mirror-symmetric populations of amacrine cells that cofasciculate with the bistratified DSGCs (Vaney et al., 1989
Our results show that as far as the spike output is concerned, the on- and off-dendritic arbors of a DSGC perform essentially the same computation but use different combinations of synaptic mechanisms. The challenge for future research is to identify the synaptic circuitry that generates the directional signals, both presynaptically in the excitatory and inhibitory neurons and postsynaptically in the DSGCs. This is the same challenge that faced Barlow et al. (1964
FOOTNOTES Received Feb. 20, 2002; revised June 10, 2002; accepted June 11, 2002.
This work was supported by National Health and Medical Research Council grants to D.I.V. and W.R.T. We thank an anonymous reviewer and Dr. Lyle Graham for their constructive criticisms that allowed us to improve this manuscript.
Correspondence should be addressed to Dr. W. Rowland Taylor, Neurological Sciences Institute, Oregon Health and Sciences University-West Campus, 505 Northwest 185th Avenue, Beaverton, OR 97006. E-mail: taylorw{at}ohsu.edu.
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M. B. Manookin, D. L. Beaudoin, Z. R. Ernst, L. J. Flagel, and J. B. Demb
Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight
J. Neurosci., April 16, 2008; 28(16): 4136 - 4150.
[Abstract] [Full Text] [PDF]
M. Kaneda, K. Ito, Y. Morishima, Y. Shigematsu, and Y. Shimoda
Characterization of Voltage-Gated Ionic Channels in Cholinergic Amacrine Cells in the Mouse Retina
J Neurophysiol, June 1, 2007; 97(6): 4225 - 4234.
[Abstract] [Full Text] [PDF]
M. van Wyk, W. R. Taylor, and D. I. Vaney
Local Edge Detectors: A Substrate for Fine Spatial Vision at Low Temporal Frequencies in Rabbit Retina
J. Neurosci., December 20, 2006; 26(51): 13250 - 13263.
[Abstract] [Full Text] [PDF]
