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A rapid and efficient learning rule for biological neural circuits

Eren Sezener, Agnieszka Grabska-Barwińska, Dimitar Kostadinov, Maxime Beau, Sanjukta Krishnagopal, David Budden, Marcus Hutter, Joel Veness, Matthew Botvinick, Claudia Clopath, Michael Häusser, Peter E. Latham
doi: https://doi.org/10.1101/2021.03.10.434756
Eren Sezener
1DeepMind
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  • For correspondence: erensezener@gmail.com
Agnieszka Grabska-Barwińska
1DeepMind
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Dimitar Kostadinov
2Wolfson Institute for Biomedical Research, University College London
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Maxime Beau
2Wolfson Institute for Biomedical Research, University College London
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Sanjukta Krishnagopal
3Gatsby Computational Neuroscience Unit, University College London
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David Budden
1DeepMind
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Marcus Hutter
1DeepMind
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Joel Veness
1DeepMind
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Matthew Botvinick
1DeepMind
3Gatsby Computational Neuroscience Unit, University College London
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Claudia Clopath
4Department of Bioengineering, Imperial College London
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Michael Häusser
2Wolfson Institute for Biomedical Research, University College London
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Peter E. Latham
3Gatsby Computational Neuroscience Unit, University College London
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Abstract

The dominant view in neuroscience is that changes in synaptic weights underlie learning. It is unclear, however, how the brain is able to determine which synapses should change, and by how much. This uncertainty stands in sharp contrast to deep learning, where changes in weights are explicitly engineered to optimize performance. However, the main tool for that, backpropagation, has two problems. One is neuro-science related: it is not biologically plausible. The other is inherent: networks trained with this rule tend to forget old tasks when learning new ones. Here we introduce the Dendritic Gated Network (DGN), a variant of the Gated Linear Network, which offers a biologically plausible alternative to backpropagation. DGNs combine dendritic ‘gating’ (whereby interneurons target dendrites to shape neuronal responses) with local learning rules to yield provably efficient performance. They are significantly more data efficient than conventional artificial networks, and are highly resistant to forgetting. Consequently, they perform well on a variety of tasks, in some cases better than backpropagation. Importantly, DGNs have structural and functional similarities to the cerebellum, a link that we strengthen by using in vivo two-photon calcium imaging to show that single interneurons suppress activity in individual dendritic branches of Purkinje cells, a key feature of the model. Thus, DGNs leverage targeted dendritic inhibition and local learning – two features ubiquitous in the brain – to achieve fast and efficient learning.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In this revised version of the manuscript, we have strengthened the link to neuroscience by performing a challenging new in vivo 2-photon imaging experiment in the cerebellum, which demonstrates that molecular layer interneurons exert strong inhibition localised to dendritic branches of single Purkinje cells - confirming a key prediction of the DGN. This is also a major result for the dendritic field, since it provides strong in vivo support for the longstanding idea that dendrites act as independent computational compartments.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 17, 2022.
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A rapid and efficient learning rule for biological neural circuits
Eren Sezener, Agnieszka Grabska-Barwińska, Dimitar Kostadinov, Maxime Beau, Sanjukta Krishnagopal, David Budden, Marcus Hutter, Joel Veness, Matthew Botvinick, Claudia Clopath, Michael Häusser, Peter E. Latham
bioRxiv 2021.03.10.434756; doi: https://doi.org/10.1101/2021.03.10.434756
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A rapid and efficient learning rule for biological neural circuits
Eren Sezener, Agnieszka Grabska-Barwińska, Dimitar Kostadinov, Maxime Beau, Sanjukta Krishnagopal, David Budden, Marcus Hutter, Joel Veness, Matthew Botvinick, Claudia Clopath, Michael Häusser, Peter E. Latham
bioRxiv 2021.03.10.434756; doi: https://doi.org/10.1101/2021.03.10.434756

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