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A high frequency resonance in the responses of retinal ganglion cells to rapidly modulated stimuli: A computer model

Published online by Cambridge University Press:  04 October 2006

J.A. MILLER ,
K.S. DENNING ,
J.S. GEORGE ,
D.W. MARSHAK  and
G.T. KENYON
J.A. MILLER
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico Neuroscience Interdepartmental Program, University of California at Los Angeles, Los Angeles, California
K.S. DENNING
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico Computational Neurobiology, University of California at San Diego, San Diego, California
J.S. GEORGE
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico
D.W. MARSHAK
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas
G.T. KENYON
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico
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Abstract

Brisk Y-type ganglion cells in the cat retina exhibit a high frequency resonance (HFR) in their responses to large, rapidly modulated stimuli. We used a computer model to test whether negative feedback mediated by axon-bearing amacrine cells onto ganglion cells could account for the experimentally observed properties of HFRs. Temporal modulation transfer functions (tMTFs) recorded from model ganglion cells exhibited HFR peaks whose amplitude, width, and locations were qualitatively consistent with experimental data. Moreover, the wide spatial distribution of axon-mediated feedback accounted for the observed increase in HFR amplitude with stimulus size. Model phase plots were qualitatively similar to those recorded from Y ganglion cells, including an anomalous phase advance that in our model coincided with the amplification of low-order harmonics that overlapped the HFR peak. When axon-mediated feedback in the model was directed primarily to bipolar cells, whose synaptic output was graded, or else when the model was replaced with a simple cascade of linear filters, it was possible to produce large HFR peaks but the region of anomalous phase advance was always eliminated, suggesting the critical involvement of strongly non-linear feedback loops. To investigate whether HFRs might contribute to visual processing, we simulated high frequency ocular tremor by rapidly modulating a naturalistic image. Visual signals riding on top of the imposed jitter conveyed an enhanced representation of large objects. We conclude that by amplifying responses to ocular tremor, HFRs may selectively enhance the processing of large image features.

Keywords

CatAlpha ganglion cellY ganglion cellAmacrine cellGap junctionSimulation
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 5 , September 2006 , pp. 779 - 794
Copyright
2006 Cambridge University Press

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