Abstract

The discovery of grid cells in the entorhinal cortex has both elucidated our understanding of spatial representations in the brain, and germinated a large number of theoretical models regarding the mechanisms of these cells’ striking spatial firing characteristics. These models cross multiple neurobiological levels that include intrinsic membrane resonance, dendritic integration, after hyperpolarization characteristics and attractor dynamics. Despite the breadth of the models, to our knowledge, parallels can be drawn between grid fields and other temporal dynamics observed in nature, much of which was described by Art Winfree and colleagues long before the initial description of grid fields. Using theoretical and mathematical investigations of oscillators, in a wide array of mediums far from the neurobiology of grid cells, Art Winfree has provided a substantial amount of research with significant and profound similarities. These theories provide specific inferences into the biological mechanisms and extraordinary resemblances across phenomenon. Therefore, this manuscript provides a novel interpretation on the phenomenon of grid fields, from the perspective of coupled oscillators, postulating that grid fields are the spatial representation of phase resetting curves in the brain. In contrast to prior models of gird cells, the current manuscript provides a sketch by which a small network of neurons, each with oscillatory components can operate to form grid cells, perhaps providing a unique hybrid between the competing attractor neural network and oscillatory interference models. The intention of this new interpretation of the data is to encourage novel testable hypotheses.

Highlights

  • ‘‘The world being made of both space and time, it proved impossible to evade embroilment in spatial patterns of timing.’’

  • While Dr Winfree contemplated the geometry of oscillators using markers, cut-outs and graph paper often distorted to make a torus, an attractor network of neurons, arranged into a torus was being implemented in a laboratory across campus at that exact moment of time in order to provide in a model of hippocampal path integration (Samsonovich and McNaughton, 1997)

  • The phenomenon of grid cells has not been described in terms of The Geometry of Biological Time (Winfree, 2001) until the present manuscript

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Summary

INTRODUCTION

‘‘The world being made of both space and time, it proved impossible to evade embroilment in spatial patterns of timing.’’. There would be thousands of neurons dedicated to the structure and support of a single torus, each with a specific size and spacing of grid fields While this issue can tenably be settled via developmental mechanisms of Hebbian plasticity (Fuhs and Touretzky, 2006), the continuous attractor neural network model does not quite explain why grid cell activity is abolished following the attenuation of the theta rhythm (Brandon et al, 2011; Koenig et al, 2011), a prominent 4–12 Hz oscillation in the hippocampus and entorhinal cortex (Jung and Kornmüller, 1938; Green and Arduini, 1954; Vanderwolf, 1969). ‘‘Viewed topologically, the new phase and the old phase are periodic coordinates, more properly represented along circles than along Cartesian coordinate axes, so the new phase-old phase plane is really the unrolled surface of a torus’’ (Winfree, 1977; Figure 4)

ART WINFREE AND THE GEOMETRY OF BIOLOGICAL TIME
THE SPATIAL GEOMETRY OF BIOLOGICAL TIME
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