The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat

Derrington, Andrew M.; Lennie, Peter

doi:10.1113/jphysiol.1982.sp014457

Cited by 155 publications

(140 citation statements)

References 28 publications

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“…The shape of the surround was unchanged by either variation. These results accord with the observation that over a wide luminance range (photopic-mesopic), receptive field structure is independent of background (29,30).…”

supporting

confidence: 90%

Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry.

Freed

Smith

Sterling

1992

Proc. Natl. Acad. Sci. U.S.A.

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The on-alpha ganglion cell in the area cen- its receptive field has a center and surround (13).Here we combine the general structure of the analytical models with detailed anatomical data to compute the contribution of the b, array to the on-alpha receptive field. The computation assumes, like the analytical models, that the on-alpha cell sums its inputs linearly. Although there are temporal nonlinearities within the on-alpha receptive field, given moderate stimulus contrast, these nonlinearities apparently sum in a spatially linear fashion (9, 11). The computation also assumes that every b, synapse evokes the same conductance increase in the on-alpha cell (for a given depolarization of the bipolar cell) and that this conductance increase depolarizes the on-alpha cell. These assumptions simplify the computation of the on-alpha receptive field to a weighted summation of bipolar receptive fields. A bipolar cell's weight depends on the number of synapses it contributes to the on-alpha dendrites and the electrotonic effects of these synapses at the soma.The receptive fields of both on and off types of alpha (Y) ganglion cells are tuned to low spatial frequencies (cutoff frequency, 2 c/degree in area centralis) (1). The Y cell contributes the major retinal input to area 18, which may explain the low-frequency tuning of this area (2, 3). The alpha cell's contribution to the visual system depends critically on the structure of its receptive field. There are two overlapping regions: a relatively broad center and a still broader antagonistic surround, each with a roughly Gaussian distribution of sensitivity (4-7).The question we address here is how does the alpha (Y) receptive field structure arise from retinal circuitry? Analytical models of the alpha receptive field give some important clues (8-11). Such models, as schematized in Fig. 1, hypothesize the receptive field to arise from a pooling of linear subunits. Each linear subunit has a center and surround with Gaussian distributions of sensitivity. These linear subunits are weighted individually and summed in a linear fashion. If appropriate distributions of sensitivity for the subunits are chosen, as well as the correct weightings, then the summed subunit centers duplicate the alpha center and the summed subunit surrounds duplicate the alpha surround (8). Although correspondence has not been established between linear subunits and any particular elements of retinal circuitry, they closely resemble, by their individual properties and their array, the bipolar cells that contact the on-alpha cell. We had previously described this source ofinput by reconstructing an on-alpha cell from serial, electron microscopic sections.Most bipolar synapses (82-89%) derive from a single bipolar METHODS An on-alpha ganglion cell from the area centralis had been filled with horseradish peroxidase, blackened with diaminobenzidine, and drawn with a camera lucida (12). Almost half of the dendritic arbor, spanning the full-field diameter, had been reconstructed by electron microsco...

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supporting

confidence: 90%

Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry.

Freed

Smith

Sterling

1992

Proc. Natl. Acad. Sci. U.S.A.

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“…In addition to the phase shift caused by temporal filtering, center and surround can have transport delays that are temporal frequency-independent. The surround delay is constrained to be larger than the center delay, as characterized in cat ganglion cells (Derrington & Lennie, 1982;Enroth-Cugell et al, 1983;Frishman et al, 1987) and those of macaque (Lee et al, 1989a;Yeh et al, 1995).…”

Section: A Model Of Chromatic-temporal Interactionmentioning

confidence: 99%

Temporal-chromatic interactions in LGN P-cells

1998

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We studied the interaction between the chromatic and temporal properties of parvocellular (P) neurons in the lateral geniculate nucleus (LGN) of macaque monkeys. We measured the amplitudes and phases of responses to stimulation by spatially uniform fields modulated sinusoidally about a white point in a three-dimensional color space, at a range of temporal frequencies between 1 and 25 Hz. Below about 4 Hz, temporal frequency had relatively little effect on chromatic tuning. At higher frequencies chromatic opponency was weakened in almost all cells. The complex interactions between temporal and chromatic properties are represented by a linear filter model that describes response amplitude and phase as a function of temporal frequency and direction in color space along which stimuli are modulated. The model stipulates the cone inputs to center and surround, their temporal properties, and the linear combination of center and surround signals. It predicts the amplitudes and phases of responses of P-cells, and the change of chromatic properties with temporal frequency. We used the model to investigate whether or not the chromatic signature of the surround in a red-green cell could be estimated from the change in the cell's chromatic properties with temporal frequency. Our findings could be equally well described by mixed cone surrounds as by pure cone surrounds, and we conclude that, with regard to temporal properties, there is no benefit to be gained by segregating cone classes in center and surround.

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“…One way is to compare the contrast sensitivity of different stages (Geisler and Davila, 1985;Geisler, 1989;Dhingra et al, 2003). The contrast detection threshold of a ganglion cell, measured in vivo and in vitro, is ϳ2-3% (Enroth-Cugell and Robson, 1966;Derrington and Lennie, 1982;Linsenmeier et al, 1982;Dhingra et al, 2003), but another stage is required for the comparison.…”

Section: Introductionmentioning

confidence: 99%

Spike Generator Limits Efficiency of Information Transfer in a Retinal Ganglion Cell

Dhingra

Smith

2004

J. Neurosci.

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The quality of the signal a retinal ganglion cell transmits to the brain is important for preception because it sets the minimum detectable stimulus. The ganglion cell converts graded potentials into a spike train with a selective filter but in the process adds noise. To explore how efficiently information is transferred to spikes, we measured contrast detection threshold and increment threshold from graded potential and spike responses of brisk-transient ganglion cells. Intracellular responses to a spot flashed over the receptive field center of the cell were recorded in an intact mammalian retina maintained in vitro at 37°C. Thresholds were measured in a single-interval forced-choice procedure with an ideal observer. The graded potential gave a detection threshold of 1.5% contrast, whereas spikes gave 3.8%. The graded potential also gave increment thresholds approximately twofold lower and carried ϳ60% more gray levels. Increment threshold "dipped" below the detection threshold at a low contrast (Ͻ5%) but increased rapidly at higher contrasts. The magnitude of the "dipper" for both graded potential and spikes could be predicted from a threshold nonlinearity in the responses. Depolarization of the cell by current injection reduced the detection threshold for spikes but also reduced the range of contrasts they can transmit. This suggests that contrast sensitivity and dynamic range are related in an essential trade-off.

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The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat

Cited by 155 publications

References 28 publications

Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry.

Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry.

Temporal-chromatic interactions in LGN P-cells

Spike Generator Limits Efficiency of Information Transfer in a Retinal Ganglion Cell

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