 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, November 15, 1999, 19(22):9756-9767
Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field
Jonathan B. Demb, Loren Haarsma, Michael A. Freed, and Peter Sterling Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6058
A retinal ganglion cell commonly expresses two spatially overlapping receptive field mechanisms. One is the familiar "center/surround," which sums excitation and inhibition across a region somewhat broader than the ganglion cell's dendritic field. This mechanism responds to a drifting grating by modulating firing at the drift frequency (linear response). Less familiar is the "nonlinear" mechanism, which sums the rectified output of many small subunits that extend for millimeters beyond the dendritic field. This mechanism responds to a contrast-reversing grating by modulating firing at twice the reversal frequency (nonlinear response). We investigated this nonlinear mechanism by presenting visual stimuli to the intact guinea pig retina in vitro while recording intracellularly from large brisk and sluggish ganglion cells. A contrast-reversing grating modulated the membrane potential (in addition to the firing rate) at twice the reversal frequency. This response was initially hyperpolarizing for some cells (either ON or OFF center) and initially depolarizing for others. Experiments in which responses to bars were summed in-phase or out-of-phase suggested that the single class of bipolar cells (either ON or OFF) that drives the center/surround response also drives the nonlinear response. Consistent with this, nonlinear responses persisted in OFF ganglion cells when ON bipolar cell responses were blocked by L-AP-4. Nonlinear responses evoked from millimeters beyond the ganglion cell were eliminated by tetrodotoxin. Thus, to relay the response from distant regions of the receptive field requires a spiking interneuron. Nonlinear responses from different regions of the receptive field added linearly.
Key words: in vitro retina; guinea pig; nonlinear subunit; shift effect; spiking amacrine cell; bipolar cell; tetrodotoxin; L-AP-4
Copyright © 1999 Society for Neuroscience 0270-6474/99/19229756-12$05.00/0
This article has been cited by other articles:
J. D. Crook, B. B. Peterson, O. S. Packer, F. R. Robinson, P. D. Gamlin, J. B. Troy, and D. M. Dacey
The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey
J. Neurosci., November 26, 2008; 28(48): 12654 - 12671.
[Abstract] [Full Text] [PDF]
D. L. Beaudoin, M. B. Manookin, and J. B. Demb
Distinct expressions of contrast gain control in parallel synaptic pathways converging on a retinal ganglion cell
J. Physiol., November 15, 2008; 586(22): 5487 - 5502.
[Abstract] [Full Text] [PDF]
J. D. Crook, B. B. Peterson, O. S. Packer, F. R. Robinson, J. B. Troy, and D. M. Dacey
Y-Cell Receptive Field and Collicular Projection of Parasol Ganglion Cells in Macaque Monkey Retina
J. Neurosci., October 29, 2008; 28(44): 11277 - 11291.
[Abstract] [Full Text] [PDF]
J. B. Demb
Functional circuitry of visual adaptation in the retina
J. Physiol., September 15, 2008; 586(18): 4377 - 4384.
[Abstract] [Full Text] [PDF]
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]
B. G. Borghuis, C. P. Ratliff, R. G. Smith, P. Sterling, and V. Balasubramanian
Design of a Neuronal Array
J. Neurosci., March 19, 2008; 28(12): 3178 - 3189.
[Abstract] [Full Text] [PDF]
D. Petrusca, M. I. Grivich, A. Sher, G. D. Field, J. L. Gauthier, M. Greschner, J. Shlens, E. J. Chichilnisky, and A. M. Litke
Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type
J. Neurosci., October 10, 2007; 27(41): 11019 - 11027.
[Abstract] [Full Text] [PDF]
K. A. Zaghloul, M. B. Manookin, B. G. Borghuis, K. Boahen, and J. B. Demb
Functional Circuitry for Peripheral Suppression in Mammalian Y-Type Retinal Ganglion Cells
J Neurophysiol, June 1, 2007; 97(6): 4327 - 4340.
[Abstract] [Full Text] [PDF]
D. L. Beaudoin, B. G. Borghuis, and J. B. Demb
Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells
J. Neurosci., March 7, 2007; 27(10): 2636 - 2645.
[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]
S. G. Solomon, B. B. Lee, and H. Sun
Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque.
J. Neurosci., August 23, 2006; 26(34): 8715 - 8726.
[Abstract] [Full Text] [PDF]
V. Bonin, V. Mante, and M. Carandini
The Suppressive Field of Neurons in Lateral Geniculate Nucleus
J. Neurosci., November 23, 2005; 25(47): 10844 - 10856.
[Abstract] [Full Text] [PDF]
M. Carandini, J. B. Demb, V. Mante, D. J. Tolhurst, Y. Dan, B. A. Olshausen, J. L. Gallant, and N. C. Rust
Do We Know What the Early Visual System Does?
J. Neurosci., November 16, 2005; 25(46): 10577 - 10597.
[Abstract] [Full Text] [PDF]
K. A. Zaghloul, K. Boahen, and J. B. Demb
Contrast Adaptation in Subthreshold and Spiking Responses of Mammalian Y-Type Retinal Ganglion Cells
J. Neurosci., January 26, 2005; 25(4): 860 - 868.
[Abstract] [Full Text] [PDF]
J. B. Demb, P. Sterling, and M. A. Freed
How Retinal Ganglion Cells Prevent Synaptic Noise From Reaching the Spike Output
J Neurophysiol, October 1, 2004; 92(4): 2510 - 2519.
[Abstract] [Full Text] [PDF]
M. J. Nolt, R. D. Kumbhani, and L. A. Palmer
Contrast-Dependent Spatial Summation in the Lateral Geniculate Nucleus and Retina of the Cat
J Neurophysiol, September 1, 2004; 92(3): 1708 - 1717.
[Abstract] [Full Text] [PDF]
M. J. McMahon, O. S. Packer, and D. M. Dacey
The Classical Receptive Field Surround of Primate Parasol Ganglion Cells Is Mediated Primarily by a Non-GABAergic Pathway
J. Neurosci., April 14, 2004; 24(15): 3736 - 3745.
[Abstract] [Full Text] [PDF]
J. R. Sinclair, A. L. Jacobs, and S. Nirenberg
Selective Ablation of a Class of Amacrine Cells Alters Spatial Processing in the Retina
J. Neurosci., February 11, 2004; 24(6): 1459 - 1467.
[Abstract] [Full Text] [PDF]
L. Diller, O. S. Packer, J. Verweij, M. J. McMahon, D. R. Williams, and D. M. Dacey
L and M Cone Contributions to the Midget and Parasol Ganglion Cell Receptive Fields of Macaque Monkey Retina
J. Neurosci., February 4, 2004; 24(5): 1079 - 1088.
[Abstract] [Full Text] [PDF]
N. K. Dhingra, Y.-H. Kao, P. Sterling, and R. G. Smith
Contrast Threshold of a Brisk-Transient Ganglion Cell In Vitro
J Neurophysiol, May 1, 2003; 89(5): 2360 - 2369.
[Abstract] [Full Text] [PDF]
K. A. Zaghloul, K. Boahen, and J. B. Demb
Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities
J. Neurosci., April 1, 2003; 23(7): 2645 - 2654.
[Abstract] [Full Text] [PDF]
M. H. Hennig, K. Funke, and F. Worgotter
The Influence of Different Retinal Subcircuits on the Nonlinearity of Ganglion Cell Behavior
J. Neurosci., October 1, 2002; 22(19): 8726 - 8738.
[Abstract] [Full Text] [PDF]
J. B. Demb, K. Zaghloul, L. Haarsma, and P. Sterling
Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina
J. Neurosci., October 1, 2001; 21(19): 7447 - 7454.
[Abstract] [Full Text] [PDF]
C. L. Passaglia, C. Enroth-Cugell, and J. B. Troy
Effects of Remote Stimulation on the Mean Firing Rate of Cat Retinal Ganglion Cells
J. Neurosci., August 1, 2001; 21(15): 5794 - 5803.
[Abstract] [Full Text] [PDF]
N. Flores-Herr, D. A. Protti, and H. Wassle
Synaptic Currents Generating the Inhibitory Surround of Ganglion Cells in the Mammalian Retina
J. Neurosci., July 1, 2001; 21(13): 4852 - 4863.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|