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. 2002 Feb 1;538(Pt 3):787-802.
doi: 10.1113/jphysiol.2001.013009.

Intrinsic physiological properties of cat retinal ganglion cells

Brendan J O'Brien  1 , Tomoki Isayama, Randal Richardson, David M Berson
Affiliations

Intrinsic physiological properties of cat retinal ganglion cells

Brendan J O'Brien et al. J Physiol. .

Abstract

Retinal ganglion cells (RGCs) are the output neurons of the retina, sending their signals via the optic nerve to many different targets in the thalamus and brainstem. These cells are divisible into more than a dozen types, differing in receptive field properties and morphology. Light responses of individual RGCs are in large part determined by the exact nature of the retinal synaptic network in which they participate. Synaptic inputs, however, are greatly influenced by the intrinsic membrane properties of each cell. While it has been demonstrated clearly that RGCs vary in their intrinsic properties, it remains unclear whether this variation is systematically related to RGC type. To learn whether membrane properties contribute to the functional differentiation of RGC types, we made whole-cell current clamp recordings of RGC responses to injected current of identified cat RGCs. The data collected demonstrated that RGC types clearly differed from one another in their intrinsic properties. One of the most striking differences we observed was that individual cell types had membrane time constants that varied widely from approximately 4 ms (alpha cells) to more than 80 ms (zeta cells). Perhaps not surprisingly, we also observed that RGCs varied greatly in their maximum spike frequencies (kappa cells 48 Hz-alpha cells 262 Hz) and sustained spike frequencies (kappa cells 23 Hz-alpha cells 67 Hz). Interestingly, however, most RGC types exhibited similar amounts of spike frequency adaptation. Finally, RGC types also differed in their responses to injection of hyperpolarizing current. Most cell types exhibited anomalous rectification in response to sufficiently strong hyperpolarization, although alpha and beta RGCs showed only minimal, if any, rectification under similar conditions. The differences we observed in RGC intrinsic properties were striking and robust. Such differences are certain to affect how each type responds to synaptic input and may help tune each cell type appropriately for their individual roles in visual processing.

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Figures

Figure 1
Figure 1. Retinal ganglion cell (RGC) types
Camera lucida drawings of cat retinal ganglion cells (RGCs) recorded by the whole-cell method. One representative recorded cell of each morphological type is shown as viewed in the wholemount (en face). Scale bar applies to all cells. Recordings from each of these cells appear in Fig. 3.
Figure 3
Figure 3. RGC spiking behaviour
Properties of action potentials and spike trains evoked in cat RGCs by depolarizing current injection. Data in each row are drawn from a single cell type. A, alpha; B, beta; C, delta; D, epsilon; E, zeta; F, eta; G, theta; H, iota; I, kappa; J, lambda. Left column, voltage responses to depolarizing current steps for a single representative cell of each morphological type. Camera lucida drawings of these cells are shown in Fig. 1. For each cell, responses are shown for three different current intensities, identified in picoamps at the right of each trace and spanning the range from near threshold (bottom) to maximal (top). Arrowheads mark pulse onset (filled) and termination (open); pulse duration, 400 ms. Numbers at bottom left in each panel indicate Vrest. Voltage scale, 50 mV. Middle column, plots of instantaneous spike frequency over time for the strongest current intensity tested that did not produce depolarization block. Panels plot data for all cells of each morphological type. Right column, plots of an index of frequency adaptation (FA index; defined in the text) as a function of normalized stimulus intensity (see text for details). For non-alpha, non-beta cells, data are shown for every cell of each type. For alpha (A3) and beta cells (B3), we plotted data for a subset of cells chosen to reflect the range of patterns evident in the entire sample; data from the selected cells are indicated in A2 and B2 by heavier lines.
Figure 2
Figure 2. Statistical analysis of intrinsic membrane properties
Comparison of morphologically identified types of cat RGCs on three intrinsic membrane properties. A, average resting membrane potential (Vrest). B, average input resistance (RN). C, average membrane time constant (τm). Error bars represent s.e.m. in this and all subsequent figures except as specified.
Figure 4
Figure 4. Statistical comparison of RGC spiking behaviour
Bar graphs summarizing population data on average spiking behaviour of cat RGC types. A, spike width (full width at half height). B, frequency adaptation (FA) index. C, maximum (filled bars) and steady-state (open bars) evoked spike frequency. Data in B and C were derived from responses to the strongest depolarizing current step tested that did not induce spike block. Maximum frequency corresponds to the reciprocal of the first interspike interval. Steady-state frequency is the reciprocal of the mean of the last three interspike intervals during the pulse. Error bars represent s.e.m. in A and B and s.d. in C.
Figure 5
Figure 5. RGC responses to hyperpolarizing current pulses
A-J, voltage responses of one cell of each morphological type to hyperpolarizing current steps (400 ms). Cells were chosen to be representative of the amount of sag typical for cells of that type. Each trace is the average of at least two individual trials. Cell type is indicated to the right of each set of traces. Voltage and time scale below panel J applies to all panels A-J. Values to the right of current pulses correspond to the maximum current step. Spikes have been clipped. K, bar graph comparing cell types on the average amplitude of sag observed when hyperpolarizing cells beyond −90 mV.
Figure 6
Figure 6. Ramping behaviour of zeta- and eta-type RGCs
Ramping behaviour illustrated in representative raw voltage records from one zeta cell (A and B) and one eta cell (C and D). A and C, response to hyperpolarizing current steps. Note the delayed return to resting potential (dotted line) upon termination of negative current pulses driving the membrane potential below −73 mV (arrows). B and D, response to depolarizing current steps during sustained negative current injection hyperpolarizing the membrane to approximately −90 mV. Note that current steps that depolarized the membrane beyond −73 mV (arrows) triggered a depolarizing ramp leading to spiking. Time and current scales are the same in all panels; current value in D (120 pA) refers to the largest pulse in that panel. The voltage scale to the right of each set of traces equals 20 mV. Spikes have been clipped in all panels.
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References

    1. Akopian A, Witkovsky P. D2 dopamine receptor-mediated inhibition of a hyperpolarization-activated current in rod photoreceptors. Journal of Neurophysiology. 1996;76:1828–1835. - PubMed
    1. Araki T, Ito M, Oshima T. Potential changes produced by application of current steps in motoneurones. Nature. 1962;191:1104–1105. - PubMed
    1. Barres BA, Silverstein BE, Corey DP, Chun LL. Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron. 1988;1:791–803. - PubMed
    1. Belluzzi O, Sacchi O, Wanke E. A fast transient outward current in the rat sympathetic neurone studied under voltage-clamp conditions. Journal of Physiology. 1985;358:91–108. - PMC - PubMed
    1. Berson DM, Isayama T, O'Brien BJ, Pu M. The kappa ganglion cell type of cat and ferret retina. Investigative Ophthalmology and Visual Science. 1999a;40:S813.

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