CaltechAUTHORS
  A Caltech Library Service

A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs

Miller, Kenneth D. (1994) A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs. Journal of Neuroscience, 14 (1). pp. 409-441. ISSN 0270-6474. PMCID PMC6576834. https://resolver.caltech.edu/CaltechAUTHORS:20191101-123859943

[img] PDF - Published Version
Creative Commons Attribution.

11Mb

Use this Persistent URL to link to this item: https://resolver.caltech.edu/CaltechAUTHORS:20191101-123859943

Abstract

Neurons in the primary visual cortex of higher mammals respond selectively to light/dark borders of a particular orientation. The receptive fields of simple cells, a type of orientation-selective cell, consist of adjacent, oriented regions alternately receiving ON-center and OFF-center excitatory input. I show that this segregation of inputs within receptive fields can occur through an activity-dependent competition between ON-center and OFF-center inputs, just as segregation of inputs between different postsynaptic cells into ocular dominance columns appears to occur through activity-dependent competition between left-eye and right-eye inputs. These different outcomes are proposed to result, not from different mechanisms, but from different spatial structures of the correlations in neural activity among the competing inputs in each case. Simple cells result if ON-center inputs are best correlated with other ON-center inputs, and OFF with OFF, at small retinotopic separations, but ON-center inputs are best correlated with OFF-center inputs at larger separations. This hypothesis leads robustly to development of simple cell receptive fields selective for orientation and spatial frequency, and to the continuous and periodic arrangement of preferred orientation across the cortex. Input correlations determine the mean preferred spatial frequency and degree of orientation selectivity. Estimates of these correlations based on measurements in adult cat retina (Mastronarde, 1983a,b) produce quantitative predictions for the mean preferred spatial frequencies of cat simple cells across eccentricities that agree with experiments (Movshon et al., 1978b). Intracortical interactions are the primary determinant of cortical organization. Simple cell spatial phases can play a key role in this organization, so arrangements of spatial phases and preferred orientations may need to be studied together to understand either alone. Possible origins for other cortical features including spatial frequency clusters, afferent ON/OFF segregation, blobs, pinwheels, and opponent inhibition within simple cell receptive fields are suggested. A number of strong experimental tests of the hypothesis are proposed.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/jneurosci.14-01-00409.1994DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6576834PubMed CentralArticle
Additional Information:© 1994 Society for Neuroscience. Received July 13, 1992; revised July 7, 1993; accepted July 13, 1993. I thank M. P. Stryker for encouraging me to take these ideas seriously at an early stage, and him and C. Koch for providing facilities and support. D. J. C. MacKay, B. Mel, E. Niebur, R. Soodak, and M. P. Stryker provided useful discussions and, along with the reviewers, helpful comments on the manuscript. B. Chapman, U. Kaplan, D. Mastronarde, M. Meister, L. Palmer, P. Schiller, and R. Wong patiently answered many questions about their experimental results. D. Mastronarde also provided a computer program needed to interpret his results. I was supported at Caltech by a Del Webb Division of Biology Fellowship, and prior to that at UCSF by an N.E.I. Fellowship. Preliminary simulations were done at the San Diego Supercomputer Center, supported by the NSF.
Funders:
Funding AgencyGrant Number
Caltech Division of BiologyUNSPECIFIED
University of California, San FranciscoUNSPECIFIED
NSFUNSPECIFIED
Subject Keywords:Hebb synapse, simple cell, ON-center cell, OFF-center cell, orientation column, orientation tuning, spatial phase, spatial frequency, visual cortex, developmental model, synaptic competition, correlations
Issue or Number:1
PubMed Central ID:PMC6576834
Record Number:CaltechAUTHORS:20191101-123859943
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191101-123859943
Official Citation:A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs. KD Miller. Journal of Neuroscience 1 January 1994, 14 (1) 409-441; DOI: 10.1523/JNEUROSCI.14-01-00409.1994
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99618
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Nov 2019 19:45
Last Modified:01 Nov 2019 19:45

Repository Staff Only: item control page