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A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity

Wörgötter, Florentin and Koch, Christof (1991) A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. Journal of Neuroscience, 11 (7). pp. 1959-1979. ISSN 0270-6474. PMCID PMC6575469. https://resolver.caltech.edu/CaltechAUTHORS:20130816-103238381

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Abstract

In order to arrive at a quantitative understanding of the dynamics of cortical neuronal networks, we simulated a detailed model of the primary visual pathway of the adult cat. This computer model comprises a 5 degrees x 5 degrees patch of the visual field at a retinal eccentricity of 4.5 degrees and includes 2048 ON- and OFF-center retinal beta-ganglion cells, 8192 geniculate X-cells, and 4096 simple cells in layer IV in area 17. The neurons are implemented as improved integrate-and-fire units. Cortical receptive fields are determined by the pattern of afferent convergence and by inhibitory intracortical connections. Orientation columns are implemented continuously with a realistic receptive field scatter and jitter in the preferred orientations. We first show that realistic ON-OFF-responses, orientation selectivity, velocity low-pass behaviour, null response, and responses to spot stimuli can be obtained with an appropriate alignment of geniculate neurons converging onto the cortical simple cell (Hubel and Wiesel, 1962) and in the absence of intracortical connections. However, the average receptive field elongation (length to width) required to obtain realistic orientation tuning is 4.0, much higher than the average observed elongation. This strongly argues for additional intracortical mechanisms sharpening orientation selectivity. In the second stage, we simulated five different inhibitory intracortical connection patterns (random, local, sparse-local, circular, and cross-orientation) in order to investigate the connection specificity necessary to achieve orientation tuning. Inhibitory connection schemes were superimposed onto Hubel and Wiesel-type receptive fields with an elongation of 1.78. Cross-orientation inhibition gave rise to different horizontal and vertical orientation tuning curves, something not observed experimentally. A combination of two inhibitory schemes, local and circular inhibition (a weak form of cross-orientation inhibition), is in good agreement with observed receptive field properties. The specificity required to establish these connections during development is low. We propose that orientation selectivity is caused by at least three different mechanisms (“eclectic” model): a weak afferent geniculate bias, broadly tuned cross-orientation inhibition, and some iso-orientation inhibition. The most surprising finding is that an isotropic connection scheme, circular inhibition, in which a cell inhibits all of its postsynaptic target cells at a distance of approximately 500 microns, enhances orientation tuning and leads to a significant directional bias. This is caused by the embedding of cortical cells within a columnar structure and does not depend on our specific assumptions.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/JNEUROSCI.11-07-01959.1991DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6575469PubMed CentralArticle
ORCID:
AuthorORCID
Koch, Christof0000-0001-6482-8067
Additional Information:© 1991 by Society for Neuroscience. Received May 16, 1990; revised Jan. 9, 1991; accepted Jan. 11, 1991. This project could never have gotten off the ground without Udo Wehmeier's skills at writing software on various machines in various languages. Matt Wilson provided help in mutating an early version of the GENESIS software into a visual cortex model. David van Essen was the midwife in charge of biological realism at the birth of this computer cat. F.W. was supported by Deutsche Forschungsgemeinschaft Grant WO-388. C.K. acknowledges support from a National Science Foundation Presidential Young Investigator Award, by grants from the Air Force Office of Scientific Research and the James S. McDonnell Foundation, and by a Bioscience Grant for International Research from the New Energy and Industrial Technology Development Organization in Japan.
Group:Koch Laboratory (KLAB)
Funders:
Funding AgencyGrant Number
Deutsche Forschungsgemeinschaft (DFG)WO-388
NSFUNSPECIFIED
Air Force Office of Scientific Research (AFOSR)UNSPECIFIED
James S. McDonnell FoundationUNSPECIFIED
New Energy and Industrial Technology Development Organization (NEDO)UNSPECIFIED
Issue or Number:7
PubMed Central ID:PMC6575469
Record Number:CaltechAUTHORS:20130816-103238381
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130816-103238381
Official Citation:A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. F Worgotter, C Koch. Journal of Neuroscience 1 July 1991, 11 (7) 1959-1979; DOI: 10.1523/JNEUROSCI.11-07-01959.1991
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:40545
Collection:CaltechAUTHORS
Deposited By: KLAB Import
Deposited On:26 Jan 2008 03:09
Last Modified:30 Oct 2019 17:27

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