Random Wiring, Ganglion Cell Mosaics, and the Functional Architecture of the Visual Cortex

PLoS Comput Biol. 2015 Nov 17;11(11):e1004602. doi: 10.1371/journal.pcbi.1004602. eCollection 2015 Nov.

Abstract

The architecture of iso-orientation domains in the primary visual cortex (V1) of placental carnivores and primates apparently follows species invariant quantitative laws. Dynamical optimization models assuming that neurons coordinate their stimulus preferences throughout cortical circuits linking millions of cells specifically predict these invariants. This might indicate that V1's intrinsic connectome and its functional architecture adhere to a single optimization principle with high precision and robustness. To validate this hypothesis, it is critical to closely examine the quantitative predictions of alternative candidate theories. Random feedforward wiring within the retino-cortical pathway represents a conceptually appealing alternative to dynamical circuit optimization because random dimension-expanding projections are believed to generically exhibit computationally favorable properties for stimulus representations. Here, we ask whether the quantitative invariants of V1 architecture can be explained as a generic emergent property of random wiring. We generalize and examine the stochastic wiring model proposed by Ringach and coworkers, in which iso-orientation domains in the visual cortex arise through random feedforward connections between semi-regular mosaics of retinal ganglion cells (RGCs) and visual cortical neurons. We derive closed-form expressions for cortical receptive fields and domain layouts predicted by the model for perfectly hexagonal RGC mosaics. Including spatial disorder in the RGC positions considerably changes the domain layout properties as a function of disorder parameters such as position scatter and its correlations across the retina. However, independent of parameter choice, we find that the model predictions substantially deviate from the layout laws of iso-orientation domains observed experimentally. Considering random wiring with the currently most realistic model of RGC mosaic layouts, a pairwise interacting point process, the predicted layouts remain distinct from experimental observations and resemble Gaussian random fields. We conclude that V1 layout invariants are specific quantitative signatures of visual cortical optimization, which cannot be explained by generic random feedforward-wiring models.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Computational Biology
  • Mammals
  • Models, Neurological*
  • Nerve Net / physiology
  • Retinal Ganglion Cells / physiology*
  • Visual Cortex / cytology*
  • Visual Cortex / physiology*

Grants and funding

This work was supported by the Human Frontier Science Program, the German Federal Ministry of Education and Research (BMBF), the German Research Foundation (DFG), the Max Planck Society (MPG), and the Volkswagen Foundation. Grant nos.: CRC 889, BFL 01GQ0921, 01GQ0922, BCCN 01GQ0430, 01GQ1005B, 01GQ07113 and BFNT 01GQ0811. This work was supported in part by the National Science Foundation, Grant no. NSF PHY11-25915. A Boehringer Ingelheim Fonds PhD fellowship to MS is gratefully acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.