Multiple bumps can enhance robustness to noise in continuous attractor networks.

A central function of continuous attractor networks is encoding coordinates and accurately updating their values through path integration. To do so, these networks produce localized bumps of activity that move coherently in response to velocity inputs. In the brain, continuous attractors are believe...

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Main Authors: Raymond Wang, Louis Kang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-10-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1010547
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author Raymond Wang
Louis Kang
author_facet Raymond Wang
Louis Kang
author_sort Raymond Wang
collection DOAJ
description A central function of continuous attractor networks is encoding coordinates and accurately updating their values through path integration. To do so, these networks produce localized bumps of activity that move coherently in response to velocity inputs. In the brain, continuous attractors are believed to underlie grid cells and head direction cells, which maintain periodic representations of position and orientation, respectively. These representations can be achieved with any number of activity bumps, and the consequences of having more or fewer bumps are unclear. We address this knowledge gap by constructing 1D ring attractor networks with different bump numbers and characterizing their responses to three types of noise: fluctuating inputs, spiking noise, and deviations in connectivity away from ideal attractor configurations. Across all three types, networks with more bumps experience less noise-driven deviations in bump motion. This translates to more robust encodings of linear coordinates, like position, assuming that each neuron represents a fixed length no matter the bump number. Alternatively, we consider encoding a circular coordinate, like orientation, such that the network distance between adjacent bumps always maps onto 360 degrees. Under this mapping, bump number does not significantly affect the amount of error in the coordinate readout. Our simulation results are intuitively explained and quantitatively matched by a unified theory for path integration and noise in multi-bump networks. Thus, to suppress the effects of biologically relevant noise, continuous attractor networks can employ more bumps when encoding linear coordinates; this advantage disappears when encoding circular coordinates. Our findings provide motivation for multiple bumps in the mammalian grid network.
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spelling doaj.art-b193bb51d70a44749470844923cc77392022-12-22T03:54:01ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-10-011810e101054710.1371/journal.pcbi.1010547Multiple bumps can enhance robustness to noise in continuous attractor networks.Raymond WangLouis KangA central function of continuous attractor networks is encoding coordinates and accurately updating their values through path integration. To do so, these networks produce localized bumps of activity that move coherently in response to velocity inputs. In the brain, continuous attractors are believed to underlie grid cells and head direction cells, which maintain periodic representations of position and orientation, respectively. These representations can be achieved with any number of activity bumps, and the consequences of having more or fewer bumps are unclear. We address this knowledge gap by constructing 1D ring attractor networks with different bump numbers and characterizing their responses to three types of noise: fluctuating inputs, spiking noise, and deviations in connectivity away from ideal attractor configurations. Across all three types, networks with more bumps experience less noise-driven deviations in bump motion. This translates to more robust encodings of linear coordinates, like position, assuming that each neuron represents a fixed length no matter the bump number. Alternatively, we consider encoding a circular coordinate, like orientation, such that the network distance between adjacent bumps always maps onto 360 degrees. Under this mapping, bump number does not significantly affect the amount of error in the coordinate readout. Our simulation results are intuitively explained and quantitatively matched by a unified theory for path integration and noise in multi-bump networks. Thus, to suppress the effects of biologically relevant noise, continuous attractor networks can employ more bumps when encoding linear coordinates; this advantage disappears when encoding circular coordinates. Our findings provide motivation for multiple bumps in the mammalian grid network.https://doi.org/10.1371/journal.pcbi.1010547
spellingShingle Raymond Wang
Louis Kang
Multiple bumps can enhance robustness to noise in continuous attractor networks.
PLoS Computational Biology
title Multiple bumps can enhance robustness to noise in continuous attractor networks.
title_full Multiple bumps can enhance robustness to noise in continuous attractor networks.
title_fullStr Multiple bumps can enhance robustness to noise in continuous attractor networks.
title_full_unstemmed Multiple bumps can enhance robustness to noise in continuous attractor networks.
title_short Multiple bumps can enhance robustness to noise in continuous attractor networks.
title_sort multiple bumps can enhance robustness to noise in continuous attractor networks
url https://doi.org/10.1371/journal.pcbi.1010547
work_keys_str_mv AT raymondwang multiplebumpscanenhancerobustnesstonoiseincontinuousattractornetworks
AT louiskang multiplebumpscanenhancerobustnesstonoiseincontinuousattractornetworks