---
OA_place: publisher
OA_type: hybrid
PlanS_conform: '1'
_id: '21378'
abstract:
- lang: eng
  text: From insects to mammals, essential brain functions, such as forming long-term
    memories (LTMs), increase metabolic activity in stimulated neurons to meet the
    energetic demand associated with brain activation. However, while impairing neuronal
    metabolism limits brain performance, whether expanding the metabolic capacity
    of neurons boosts brain function remains poorly understood. Here, we show that
    LTM formation of flies and mice can be enhanced by increasing mitochondrial metabolism
    in central memory circuits. By knocking down the mitochondrial Ca2+ exporter Letm1,
    we favour Ca2+ retention in the mitochondrial matrix of neurons due to reduction
    of mitochondrial H+/Ca2+ exchange. The resulting increase in mitochondrial Ca2+
    over-activates mitochondrial metabolism in neurons of central memory circuits,
    leading to improved LTM storage in training paradigms in which wild-type counterparts
    of both species fail to remember. Our findings unveil an evolutionarily conserved
    mechanism that controls mitochondrial metabolism in neurons and indicate its involvement
    in shaping higher brain functions, such as LTM.
acknowledgement: We thank all members of the laboratory of J.d.J.-S. for insightful
  discussions and comments. We thank S. Perez for technical assistance. This work
  was made possible by the Paris Brain Institute Diane Barriere Chair in Synaptic
  Bioenergetics awarded to J.d.J.-S., who is also supported by an ERC Starting Grant
  (SynaptoEnergy, European Research Council; ERC-StG-852873), 2019 ATIP-Avenir Grant
  (CNRS, Inserm), a Big Brain Theory Grant (ICM Foundation) and a Kavli Exploratory
  Award (Kavli Foundation). This work was also supported by an ERC Advanced Grant
  (EnergyMeMo; ERC-AdG-741550) to T.P. and grants from the Agence Nationale de la
  Recherche to P.Y.P. (ANR-20-CE92-0047-01), T.P. (ANR-23-CE16-0029-01), A.P. and
  J.d.J.-S. (ANR-22-CE16-0020) and J.d.J.-S. (ANR-24-CE16-0221). T.P., P.Y.P. and
  J.d.J.-S. are permanent CNRS researchers. A.P. is a permanent ESPCI associate professor.
  T.C. was funded by the French Ministry of Research and the Fondation pour la Recherche
  Médicale. V.R. was funded by the Max Planck Society, the Chan Zuckerberg Initiative
  DAF, an advised fund of the Silicon Valley Community Foundation grant number 2024-349543
  and the NIH Director’s New Innovator Award (DP2 MH140148). A.B.-G. and C.R.-D. received
  funding from an ERC Starting Grant (HighMemory; ERC-StG-948217), the Ministry of
  Economy and Competitiveness (PID2021-122795OB-I00) and the Departament d’Economia
  i Coneixement de la Generalitat de Catalunya (SGR 00022). T.P.V. was funded by the
  Wellcome Trust and a Royal Society Sir Henry Dale Research Fellowship (WT100000)
  and a Wellcome Trust Senior Research Fellowship (214316/Z/18/Z). K.G. was supported
  by the DIM C-BRAINS, funded by the Conseil Régional d’Ile-de-France. The contributions
  of H.F. and E.R.S. were supported by the Howard Hughes Medical Institute. The PHENO-ICMice
  animal Core at ICM is supported by two ‘Investissements d’avenir’ (ANR-10- IAIHU-06
  and ANR-11-INBS-0011-NeurATRIS) and the Fondation pour la Recherche Médicale.
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Anjali
  full_name: Amrapali Vishwanath, Anjali
  last_name: Amrapali Vishwanath
- first_name: Typhaine
  full_name: Comyn, Typhaine
  last_name: Comyn
- first_name: Rodrigo G.
  full_name: Mira, Rodrigo G.
  last_name: Mira
- first_name: Claire
  full_name: Brossier, Claire
  last_name: Brossier
- first_name: Carlos
  full_name: Pascual-Caro, Carlos
  last_name: Pascual-Caro
- first_name: Maya
  full_name: Faour, Maya
  last_name: Faour
- first_name: Kahina
  full_name: Boumendil, Kahina
  last_name: Boumendil
- first_name: Chaitanya
  full_name: Chintaluri, Chaitanya
  id: BA06AFEE-A4BA-11EA-AE5C-14673DDC885E
  last_name: Chintaluri
  orcid: 0000-0003-4252-1608
- first_name: Carla
  full_name: Ramon-Duaso, Carla
  last_name: Ramon-Duaso
- first_name: Ruolin
  full_name: Fan, Ruolin
  last_name: Fan
- first_name: Kishalay
  full_name: Ghosh, Kishalay
  last_name: Ghosh
- first_name: Helen
  full_name: Farrants, Helen
  last_name: Farrants
- first_name: Jean-Paul
  full_name: Berwick, Jean-Paul
  last_name: Berwick
- first_name: Riya
  full_name: Sivakumar, Riya
  last_name: Sivakumar
- first_name: Mario
  full_name: Lopez-Manzaneda, Mario
  last_name: Lopez-Manzaneda
- first_name: Eric R.
  full_name: Schreiter, Eric R.
  last_name: Schreiter
- first_name: Thomas
  full_name: Preat, Thomas
  last_name: Preat
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
- first_name: Vidhya
  full_name: Rangaraju, Vidhya
  last_name: Rangaraju
- first_name: Arnau
  full_name: Busquets-Garcia, Arnau
  last_name: Busquets-Garcia
- first_name: Pierre-Yves
  full_name: Plaçais, Pierre-Yves
  last_name: Plaçais
- first_name: Alice
  full_name: Pavlowsky, Alice
  last_name: Pavlowsky
- first_name: Jaime
  full_name: de Juan-Sanz, Jaime
  last_name: de Juan-Sanz
citation:
  ama: Amrapali Vishwanath A, Comyn T, Mira RG, et al. Mitochondrial Ca2+ efflux controls
    neuronal metabolism and long-term memory across species. <i>Nature Metabolism</i>.
    2026;8(2):467-488. doi:<a href="https://doi.org/10.1038/s42255-026-01451-w">10.1038/s42255-026-01451-w</a>
  apa: Amrapali Vishwanath, A., Comyn, T., Mira, R. G., Brossier, C., Pascual-Caro,
    C., Faour, M., … de Juan-Sanz, J. (2026). Mitochondrial Ca2+ efflux controls neuronal
    metabolism and long-term memory across species. <i>Nature Metabolism</i>. Springer
    Nature. <a href="https://doi.org/10.1038/s42255-026-01451-w">https://doi.org/10.1038/s42255-026-01451-w</a>
  chicago: Amrapali Vishwanath, Anjali, Typhaine Comyn, Rodrigo G. Mira, Claire Brossier,
    Carlos Pascual-Caro, Maya Faour, Kahina Boumendil, et al. “Mitochondrial Ca2+
    Efflux Controls Neuronal Metabolism and Long-Term Memory across Species.” <i>Nature
    Metabolism</i>. Springer Nature, 2026. <a href="https://doi.org/10.1038/s42255-026-01451-w">https://doi.org/10.1038/s42255-026-01451-w</a>.
  ieee: A. Amrapali Vishwanath <i>et al.</i>, “Mitochondrial Ca2+ efflux controls
    neuronal metabolism and long-term memory across species,” <i>Nature Metabolism</i>,
    vol. 8, no. 2. Springer Nature, pp. 467–488, 2026.
  ista: Amrapali Vishwanath A, Comyn T, Mira RG, Brossier C, Pascual-Caro C, Faour
    M, Boumendil K, Chintaluri C, Ramon-Duaso C, Fan R, Ghosh K, Farrants H, Berwick
    J-P, Sivakumar R, Lopez-Manzaneda M, Schreiter ER, Preat T, Vogels TP, Rangaraju
    V, Busquets-Garcia A, Plaçais P-Y, Pavlowsky A, de Juan-Sanz J. 2026. Mitochondrial
    Ca2+ efflux controls neuronal metabolism and long-term memory across species.
    Nature Metabolism. 8(2), 467–488.
  mla: Amrapali Vishwanath, Anjali, et al. “Mitochondrial Ca2+ Efflux Controls Neuronal
    Metabolism and Long-Term Memory across Species.” <i>Nature Metabolism</i>, vol.
    8, no. 2, Springer Nature, 2026, pp. 467–88, doi:<a href="https://doi.org/10.1038/s42255-026-01451-w">10.1038/s42255-026-01451-w</a>.
  short: A. Amrapali Vishwanath, T. Comyn, R.G. Mira, C. Brossier, C. Pascual-Caro,
    M. Faour, K. Boumendil, C. Chintaluri, C. Ramon-Duaso, R. Fan, K. Ghosh, H. Farrants,
    J.-P. Berwick, R. Sivakumar, M. Lopez-Manzaneda, E.R. Schreiter, T. Preat, T.P.
    Vogels, V. Rangaraju, A. Busquets-Garcia, P.-Y. Plaçais, A. Pavlowsky, J. de Juan-Sanz,
    Nature Metabolism 8 (2026) 467–488.
date_created: 2026-03-02T10:04:49Z
date_published: 2026-02-11T00:00:00Z
date_updated: 2026-03-02T15:23:10Z
day: '11'
ddc:
- '570'
department:
- _id: TiVo
doi: 10.1038/s42255-026-01451-w
external_id:
  pmid:
  - '41673453'
file:
- access_level: open_access
  checksum: 365932a599d05bc9ce8a57204e7a1465
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  creator: dernst
  date_created: 2026-03-02T15:21:27Z
  date_updated: 2026-03-02T15:21:27Z
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  file_size: 5326608
  relation: main_file
  success: 1
file_date_updated: 2026-03-02T15:21:27Z
has_accepted_license: '1'
intvolume: '         8'
issue: '2'
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 467-488
pmid: 1
project:
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: What’s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks.
publication: Nature Metabolism
publication_identifier:
  eissn:
  - 2522-5812
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Mitochondrial Ca2+ efflux controls neuronal metabolism and long-term memory
  across species
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 8
year: '2026'
...
---
OA_place: publisher
OA_type: gold
_id: '8125'
abstract:
- lang: eng
  text: "Biological memory is known to be flexible—memory formation and recall depend
    on factors such as the behavioral context of the organism. However, this property
    is often ignored in associative memory models, leaving it unclear how memories
    can be organized and recalled when subject to contextual control. Because of the
    lack of a rigorous analytical framework, it is also unknown how contextual control
    affects memory stability, storage capacity, and information content. Here, we
    bring the dynamic nature of memory to the fore by introducing a novel model of
    associative memory, which we refer to as the context-modular memory network. In
    our model, stored memory patterns are associated to one of several background
    network states, or contexts. Memories are accessible when their corresponding
    context is active, and are otherwise inaccessible. Context modulates the effective
    network connectivity by imposing a specific\r\nconfiguration of neuronal and synaptic
    gating—gated neurons (synapses) have their activity (weights) momentarily silenced,
    thereby reducing interference from memories belonging to other contexts. Memory
    patterns are randomly and independently chosen, while neuronal and synaptic gates
    may be selected randomly or optimized through a process of contextual synaptic
    refinement. Through analytic and numerical results, we show that context-modular
    memory networks can exhibit both improved memory capacity and differential control
    of memory stability with random gating (especially for neuronal gating). For contextual
    synaptic refinement, we devise a method in which synapses are gated off for a
    given context if they destabilize the memory patterns in that context, drastically
    improving memory capacity and enabling even more precise control over memory stability.
    Notably, synaptic refinement allows for patterns to be\r\naccessible in multiple
    contexts, stabilizing memory patterns even for weight matrices that alone do not
    contain any information about the memory patterns, such as Gaussian random matrices.
    Overall, our model integrates recent ideas about context-dependent memory organization
    with classic associative memory models and proposes a rigorous theory which can
    act as a framework for future work. Furthermore, our work carries important implications
    for the understanding of biological memory storage and recall in the brain, such
    as highlighting an intriguing trade-off between memory capacity and accessibility."
acknowledgement: "We thank Helen Barron, Vezha Boboeva, Adam Packer, João Sacramento,
  Andrew Saxe, Misha Tsodyks, and Friedemann Zenke for helpful comments at various
  stages of this work, and Rubem Erichsen, Jr. for carefully reading the manuscript
  and valuable comments. This work was\r\nsupported by a Sir Henry Dale Fellowship
  by the Wellcome Trust and the Royal Society [No. WT100000 (W. F. P., E. J. A., and
  T. P. V.)], a Wellcome Trust Senior Research Fellowship [No. 214316/Z/18/Z (E. J.
  A. and T. P. V.)], and a Research Project Grant by the Leverhulme Trust\r\n[No.
  RPG-2016-446 (E. J. A.)]. "
article_number: '011057'
article_processing_charge: Yes
article_type: original
author:
- first_name: William F.
  full_name: Podlaski, William F.
  last_name: Podlaski
  orcid: 0000-0001-6619-7502
- first_name: Everton J.
  full_name: Agnes, Everton J.
  last_name: Agnes
  orcid: 0000-0001-7184-7311
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: Podlaski WF, Agnes EJ, Vogels TP. High capacity and dynamic accessibility in
    associative memory networks with context-dependent neuronal and synaptic gating.
    <i>Physical Review X</i>. 2025;15. doi:<a href="https://doi.org/10.1103/PhysRevX.15.011057">10.1103/PhysRevX.15.011057</a>
  apa: Podlaski, W. F., Agnes, E. J., &#38; Vogels, T. P. (2025). High capacity and
    dynamic accessibility in associative memory networks with context-dependent neuronal
    and synaptic gating. <i>Physical Review X</i>. American Physical Society. <a href="https://doi.org/10.1103/PhysRevX.15.011057">https://doi.org/10.1103/PhysRevX.15.011057</a>
  chicago: Podlaski, William F., Everton J. Agnes, and Tim P Vogels. “High Capacity
    and Dynamic Accessibility in Associative Memory Networks with Context-Dependent
    Neuronal and Synaptic Gating.” <i>Physical Review X</i>. American Physical Society,
    2025. <a href="https://doi.org/10.1103/PhysRevX.15.011057">https://doi.org/10.1103/PhysRevX.15.011057</a>.
  ieee: W. F. Podlaski, E. J. Agnes, and T. P. Vogels, “High capacity and dynamic
    accessibility in associative memory networks with context-dependent neuronal and
    synaptic gating,” <i>Physical Review X</i>, vol. 15. American Physical Society,
    2025.
  ista: Podlaski WF, Agnes EJ, Vogels TP. 2025. High capacity and dynamic accessibility
    in associative memory networks with context-dependent neuronal and synaptic gating.
    Physical Review X. 15, 011057.
  mla: Podlaski, William F., et al. “High Capacity and Dynamic Accessibility in Associative
    Memory Networks with Context-Dependent Neuronal and Synaptic Gating.” <i>Physical
    Review X</i>, vol. 15, 011057, American Physical Society, 2025, doi:<a href="https://doi.org/10.1103/PhysRevX.15.011057">10.1103/PhysRevX.15.011057</a>.
  short: W.F. Podlaski, E.J. Agnes, T.P. Vogels, Physical Review X 15 (2025).
corr_author: '1'
date_created: 2020-07-16T12:24:28Z
date_published: 2025-03-13T00:00:00Z
date_updated: 2025-05-19T13:51:27Z
day: '13'
ddc:
- '530'
department:
- _id: TiVo
doi: 10.1103/PhysRevX.15.011057
external_id:
  isi:
  - '001451378900002'
file:
- access_level: open_access
  checksum: 1f27ee469ab51a3e1ce1e2df0022e81d
  content_type: application/pdf
  creator: dernst
  date_created: 2025-03-20T12:47:17Z
  date_updated: 2025-03-20T12:47:17Z
  file_id: '19432'
  file_name: 2025_PhysReviewX_Podlaski.pdf
  file_size: 1373704
  relation: main_file
  success: 1
file_date_updated: 2025-03-20T12:47:17Z
has_accepted_license: '1'
intvolume: '        15'
isi: 1
language:
- iso: eng
locked: '1'
month: '03'
oa: 1
oa_version: Published Version
project:
- _id: B67AFEDC-15C9-11EA-A837-991A96BB2854
  name: IST Austria Open Access Fund
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: What’s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks.
publication: Physical Review X
publication_identifier:
  eissn:
  - 2160-3308
publication_status: published
publisher: American Physical Society
quality_controlled: '1'
related_material:
  link:
  - relation: software
    url: https://github.com/wpodlaski/contextual-memory-nets
scopus_import: '1'
status: public
title: High capacity and dynamic accessibility in associative memory networks with
  context-dependent neuronal and synaptic gating
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 15
year: '2025'
...
---
OA_place: publisher
OA_type: hybrid
_id: '14666'
abstract:
- lang: eng
  text: So-called spontaneous activity is a central hallmark of most nervous systems.
    Such non-causal firing is contrary to the tenet of spikes as a means of communication,
    and its purpose remains unclear. We propose that self-initiated firing can serve
    as a release valve to protect neurons from the toxic conditions arising in mitochondria
    from lower-than-baseline energy consumption. To demonstrate the viability of our
    hypothesis, we built a set of models that incorporate recent experimental results
    indicating homeostatic control of metabolic products—Adenosine triphosphate (ATP),
    adenosine diphosphate (ADP), and reactive oxygen species (ROS)—by changes in firing.
    We explore the relationship of metabolic cost of spiking with its effect on the
    temporal patterning of spikes and reproduce experimentally observed changes in
    intrinsic firing in the fruitfly dorsal fan-shaped body neuron in a model with
    ROS-modulated potassium channels. We also show that metabolic spiking homeostasis
    can produce indefinitely sustained avalanche dynamics in cortical circuits. Our
    theory can account for key features of neuronal activity observed in many studies
    ranging from ion channel function all the way to resting state dynamics. We finish
    with a set of experimental predictions that would confirm an integrated, crucial
    role for metabolically regulated spiking and firmly link metabolic homeostasis
    and neuronal function.
acknowledgement: We thank Prof. C. Nazaret and Prof. J.-P. Mazat for sharing the code
  of their mitochondrial model. We also thank G. Miesenböck, E. Marder, L. Abbott,
  A. Kempf, P. Hasenhuetl, W. Podlaski, F. Zenke, E. Agnes, P. Bozelos, J. Watson,
  B. Confavreux, and G. Christodoulou, and the rest of the Vogels Lab for their feedback.
  This work was funded by Wellcome Trust and Royal Society Sir Henry Dale Research
  Fellowship (WT100000), a Wellcome Trust Senior Research Fellowship (214316/Z/18/Z),
  and a UK Research and Innovation, Biotechnology and Biological Sciences Research
  Council grant (UKRI-BBSRC BB/N019512/1).
article_number: e2306525120
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Chaitanya
  full_name: Chintaluri, Chaitanya
  id: E4EDB536-3485-11EA-98D2-20AF3DDC885E
  last_name: Chintaluri
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: Chintaluri C, Vogels TP. Metabolically regulated spiking could serve neuronal
    energy homeostasis and protect from reactive oxygen species. <i>Proceedings of
    the National Academy of Sciences of the United States of America</i>. 2023;120(48).
    doi:<a href="https://doi.org/10.1073/pnas.2306525120">10.1073/pnas.2306525120</a>
  apa: Chintaluri, C., &#38; Vogels, T. P. (2023). Metabolically regulated spiking
    could serve neuronal energy homeostasis and protect from reactive oxygen species.
    <i>Proceedings of the National Academy of Sciences of the United States of America</i>.
    National Academy of Sciences. <a href="https://doi.org/10.1073/pnas.2306525120">https://doi.org/10.1073/pnas.2306525120</a>
  chicago: Chintaluri, Chaitanya, and Tim P Vogels. “Metabolically Regulated Spiking
    Could Serve Neuronal Energy Homeostasis and Protect from Reactive Oxygen Species.”
    <i>Proceedings of the National Academy of Sciences of the United States of America</i>.
    National Academy of Sciences, 2023. <a href="https://doi.org/10.1073/pnas.2306525120">https://doi.org/10.1073/pnas.2306525120</a>.
  ieee: C. Chintaluri and T. P. Vogels, “Metabolically regulated spiking could serve
    neuronal energy homeostasis and protect from reactive oxygen species,” <i>Proceedings
    of the National Academy of Sciences of the United States of America</i>, vol.
    120, no. 48. National Academy of Sciences, 2023.
  ista: Chintaluri C, Vogels TP. 2023. Metabolically regulated spiking could serve
    neuronal energy homeostasis and protect from reactive oxygen species. Proceedings
    of the National Academy of Sciences of the United States of America. 120(48),
    e2306525120.
  mla: Chintaluri, Chaitanya, and Tim P. Vogels. “Metabolically Regulated Spiking
    Could Serve Neuronal Energy Homeostasis and Protect from Reactive Oxygen Species.”
    <i>Proceedings of the National Academy of Sciences of the United States of America</i>,
    vol. 120, no. 48, e2306525120, National Academy of Sciences, 2023, doi:<a href="https://doi.org/10.1073/pnas.2306525120">10.1073/pnas.2306525120</a>.
  short: C. Chintaluri, T.P. Vogels, Proceedings of the National Academy of Sciences
    of the United States of America 120 (2023).
corr_author: '1'
date_created: 2023-12-10T23:01:00Z
date_published: 2023-11-21T00:00:00Z
date_updated: 2025-09-24T11:16:56Z
day: '21'
ddc:
- '570'
department:
- _id: TiVo
doi: 10.1073/pnas.2306525120
external_id:
  isi:
  - '001157389000005'
  pmid:
  - '37988463'
file:
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  checksum: bf4ec38602a70dae4338077a5a4d497f
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  creator: dernst
  date_created: 2023-12-11T12:45:12Z
  date_updated: 2023-12-11T12:45:12Z
  file_id: '14678'
  file_name: 2023_PNAS_Chintaluri.pdf
  file_size: 16891602
  relation: main_file
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file_date_updated: 2023-12-11T12:45:12Z
has_accepted_license: '1'
intvolume: '       120'
isi: 1
issue: '48'
language:
- iso: eng
month: '11'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: What’s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks.
publication: Proceedings of the National Academy of Sciences of the United States
  of America
publication_identifier:
  eissn:
  - 1091-6490
  issn:
  - 0027-8424
publication_status: published
publisher: National Academy of Sciences
quality_controlled: '1'
related_material:
  link:
  - relation: software
    url: https://github.com/ccluri/metabolic_spiking
scopus_import: '1'
status: public
title: Metabolically regulated spiking could serve neuronal energy homeostasis and
  protect from reactive oxygen species
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 120
year: '2023'
...
---
_id: '12009'
abstract:
- lang: eng
  text: Changes in the short-term dynamics of excitatory synapses over development
    have been observed throughout cortex, but their purpose and consequences remain
    unclear. Here, we propose that developmental changes in synaptic dynamics buffer
    the effect of slow inhibitory long-term plasticity, allowing for continuously
    stable neural activity. Using computational modeling we demonstrate that early
    in development excitatory short-term depression quickly stabilises neural activity,
    even in the face of strong, unbalanced excitation. We introduce a model of the
    commonly observed developmental shift from depression to facilitation and show
    that neural activity remains stable throughout development, while inhibitory synaptic
    plasticity slowly balances excitation, consistent with experimental observations.
    Our model predicts changes in the input responses from phasic to phasic-and-tonic
    and more precise spike timings. We also observe a gradual emergence of short-lasting
    memory traces governed by short-term plasticity development. We conclude that
    the developmental depression-to-facilitation shift may control excitation-inhibition
    balance throughout development with important functional consequences.
acknowledgement: We would like to thank the Vogels Lab for feedback on an earlier
  version of this manuscript. D.W.J. was supported by a Marshall Scholarship and a
  Clarendon Scholarship. R.P.C. and T.P.V. were supported by a Wellcome Trust and
  Royal Society Sir Henry Dale Fellowship (WT 100000), a Wellcome Trust Senior Research
  Fellowship (214316/Z/18/Z), and an ERC Consolidator Grant (SYNAPSEEK).
article_number: '873'
article_processing_charge: No
article_type: original
author:
- first_name: David W.
  full_name: Jia, David W.
  last_name: Jia
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
- first_name: Rui Ponte
  full_name: Costa, Rui Ponte
  last_name: Costa
citation:
  ama: Jia DW, Vogels TP, Costa RP. Developmental depression-to-facilitation shift
    controls excitation-inhibition balance. <i>Communications biology</i>. 2022;5.
    doi:<a href="https://doi.org/10.1038/s42003-022-03801-2">10.1038/s42003-022-03801-2</a>
  apa: Jia, D. W., Vogels, T. P., &#38; Costa, R. P. (2022). Developmental depression-to-facilitation
    shift controls excitation-inhibition balance. <i>Communications Biology</i>. Springer
    Nature. <a href="https://doi.org/10.1038/s42003-022-03801-2">https://doi.org/10.1038/s42003-022-03801-2</a>
  chicago: Jia, David W., Tim P Vogels, and Rui Ponte Costa. “Developmental Depression-to-Facilitation
    Shift Controls Excitation-Inhibition Balance.” <i>Communications Biology</i>.
    Springer Nature, 2022. <a href="https://doi.org/10.1038/s42003-022-03801-2">https://doi.org/10.1038/s42003-022-03801-2</a>.
  ieee: D. W. Jia, T. P. Vogels, and R. P. Costa, “Developmental depression-to-facilitation
    shift controls excitation-inhibition balance,” <i>Communications biology</i>,
    vol. 5. Springer Nature, 2022.
  ista: Jia DW, Vogels TP, Costa RP. 2022. Developmental depression-to-facilitation
    shift controls excitation-inhibition balance. Communications biology. 5, 873.
  mla: Jia, David W., et al. “Developmental Depression-to-Facilitation Shift Controls
    Excitation-Inhibition Balance.” <i>Communications Biology</i>, vol. 5, 873, Springer
    Nature, 2022, doi:<a href="https://doi.org/10.1038/s42003-022-03801-2">10.1038/s42003-022-03801-2</a>.
  short: D.W. Jia, T.P. Vogels, R.P. Costa, Communications Biology 5 (2022).
date_created: 2022-09-04T22:02:02Z
date_published: 2022-08-25T00:00:00Z
date_updated: 2025-04-14T09:44:14Z
day: '25'
ddc:
- '570'
department:
- _id: TiVo
doi: 10.1038/s42003-022-03801-2
ec_funded: 1
external_id:
  isi:
  - '000844814800007'
file:
- access_level: open_access
  checksum: 3ec724c4f6d3440028c217305e32915f
  content_type: application/pdf
  creator: dernst
  date_created: 2022-09-05T08:55:11Z
  date_updated: 2022-09-05T08:55:11Z
  file_id: '12022'
  file_name: 2022_CommBiology_Jia.pdf
  file_size: 2491191
  relation: main_file
  success: 1
file_date_updated: 2022-09-05T08:55:11Z
has_accepted_license: '1'
intvolume: '         5'
isi: 1
language:
- iso: eng
month: '08'
oa: 1
oa_version: Published Version
project:
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: "Whatâ\x80\x99s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks."
- _id: 0aacfa84-070f-11eb-9043-d7eb2c709234
  call_identifier: H2020
  grant_number: '819603'
  name: Learning the shape of synaptic plasticity rules for neuronal architectures
    and function through machine learning.
publication: Communications biology
publication_identifier:
  eissn:
  - 2399-3642
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Developmental depression-to-facilitation shift controls excitation-inhibition
  balance
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 5
year: '2022'
...
---
_id: '12084'
abstract:
- lang: eng
  text: Neuronal networks encode information through patterns of activity that define
    the networks’ function. The neurons’ activity relies on specific connectivity
    structures, yet the link between structure and function is not fully understood.
    Here, we tackle this structure-function problem with a new conceptual approach.
    Instead of manipulating the connectivity directly, we focus on upper triangular
    matrices, which represent the network dynamics in a given orthonormal basis obtained
    by the Schur decomposition. This abstraction allows us to independently manipulate
    the eigenspectrum and feedforward structures of a connectivity matrix. Using this
    method, we describe a diverse repertoire of non-normal transient amplification,
    and to complement the analysis of the dynamical regimes, we quantify the geometry
    of output trajectories through the effective rank of both the eigenvector and
    the dynamics matrices. Counter-intuitively, we find that shrinking the eigenspectrum’s
    imaginary distribution leads to highly amplifying regimes in linear and long-lasting
    dynamics in nonlinear networks. We also find a trade-off between amplification
    and dimensionality of neuronal dynamics, i.e., trajectories in neuronal state-space.
    Networks that can amplify a large number of orthogonal initial conditions produce
    neuronal trajectories that lie in the same subspace of the neuronal state-space.
    Finally, we examine networks of excitatory and inhibitory neurons. We find that
    the strength of global inhibition is directly linked with the amplitude of amplification,
    such that weakening inhibitory weights also decreases amplification, and that
    the eigenspectrum’s imaginary distribution grows with an increase in the ratio
    between excitatory-to-inhibitory and excitatory-to-excitatory connectivity strengths.
    Consequently, the strength of global inhibition reveals itself as a strong signature
    for amplification and a potential control mechanism to switch dynamical regimes.
    Our results shed a light on how biological networks, i.e., networks constrained
    by Dale’s law, may be optimised for specific dynamical regimes.
acknowledgement: 'We thank Friedemann Zenke for his comments, especially on the effect
  of the self loops on the spectrum. We also thank Ken Miller and Bill Podlaski for
  helpful comments. This research was funded by a Wellcome Trust and Royal Society
  Henry Dale Research Fellowship (WT100000; TPV), a Wellcome Senior Research Fellowship
  (214316/Z/18/Z; GC, EJA, and TPV), and a Research Project Grant by the Leverhulme
  Trust (RPG-2016-446; EJA and TPV). '
article_number: e1010365
article_processing_charge: No
article_type: original
author:
- first_name: Georgia
  full_name: Christodoulou, Georgia
  last_name: Christodoulou
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
- first_name: Everton J.
  full_name: Agnes, Everton J.
  last_name: Agnes
citation:
  ama: Christodoulou G, Vogels TP, Agnes EJ. Regimes and mechanisms of transient amplification
    in abstract and biological neural networks. <i>PLoS Computational Biology</i>.
    2022;18(8). doi:<a href="https://doi.org/10.1371/journal.pcbi.1010365">10.1371/journal.pcbi.1010365</a>
  apa: Christodoulou, G., Vogels, T. P., &#38; Agnes, E. J. (2022). Regimes and mechanisms
    of transient amplification in abstract and biological neural networks. <i>PLoS
    Computational Biology</i>. Public Library of Science. <a href="https://doi.org/10.1371/journal.pcbi.1010365">https://doi.org/10.1371/journal.pcbi.1010365</a>
  chicago: Christodoulou, Georgia, Tim P Vogels, and Everton J. Agnes. “Regimes and
    Mechanisms of Transient Amplification in Abstract and Biological Neural Networks.”
    <i>PLoS Computational Biology</i>. Public Library of Science, 2022. <a href="https://doi.org/10.1371/journal.pcbi.1010365">https://doi.org/10.1371/journal.pcbi.1010365</a>.
  ieee: G. Christodoulou, T. P. Vogels, and E. J. Agnes, “Regimes and mechanisms of
    transient amplification in abstract and biological neural networks,” <i>PLoS Computational
    Biology</i>, vol. 18, no. 8. Public Library of Science, 2022.
  ista: Christodoulou G, Vogels TP, Agnes EJ. 2022. Regimes and mechanisms of transient
    amplification in abstract and biological neural networks. PLoS Computational Biology.
    18(8), e1010365.
  mla: Christodoulou, Georgia, et al. “Regimes and Mechanisms of Transient Amplification
    in Abstract and Biological Neural Networks.” <i>PLoS Computational Biology</i>,
    vol. 18, no. 8, e1010365, Public Library of Science, 2022, doi:<a href="https://doi.org/10.1371/journal.pcbi.1010365">10.1371/journal.pcbi.1010365</a>.
  short: G. Christodoulou, T.P. Vogels, E.J. Agnes, PLoS Computational Biology 18
    (2022).
corr_author: '1'
date_created: 2022-09-11T22:01:56Z
date_published: 2022-08-15T00:00:00Z
date_updated: 2025-06-11T13:51:21Z
day: '15'
ddc:
- '570'
department:
- _id: TiVo
doi: 10.1371/journal.pcbi.1010365
external_id:
  isi:
  - '000937227700001'
  pmid:
  - '35969604'
file:
- access_level: open_access
  checksum: 8a81ab29f837991ee0ea770817c4a50e
  content_type: application/pdf
  creator: dernst
  date_created: 2022-09-12T07:47:55Z
  date_updated: 2022-09-12T07:47:55Z
  file_id: '12090'
  file_name: 2022_PLoSCompBio_Christodoulou.pdf
  file_size: 2867337
  relation: main_file
  success: 1
file_date_updated: 2022-09-12T07:47:55Z
has_accepted_license: '1'
intvolume: '        18'
isi: 1
issue: '8'
language:
- iso: eng
month: '08'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: "Whatâ\x80\x99s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks."
publication: PLoS Computational Biology
publication_identifier:
  eissn:
  - 1553-7358
publication_status: published
publisher: Public Library of Science
quality_controlled: '1'
scopus_import: '1'
status: public
title: Regimes and mechanisms of transient amplification in abstract and biological
  neural networks
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 18
year: '2022'
...
---
_id: '11453'
abstract:
- lang: eng
  text: "Neuronal computations depend on synaptic connectivity and intrinsic electrophysiological
    properties. Synaptic connectivity determines which inputs from presynaptic neurons
    are integrated, while cellular properties determine how inputs are filtered over
    time. Unlike their biological counterparts, most computational approaches to learning
    in simulated neural networks are limited to changes in synaptic connectivity.
    However, if intrinsic parameters change, neural computations are altered drastically.
    Here, we include the parameters that determine the intrinsic properties,\r\ne.g.,
    time constants and reset potential, into the learning paradigm. Using sparse feedback
    signals that indicate target spike times, and gradient-based parameter updates,
    we show that the intrinsic parameters can be learned along with the synaptic weights
    to produce specific input-output functions. Specifically, we use a teacher-student
    paradigm in which a randomly initialised leaky integrate-and-fire or resonate-and-fire
    neuron must recover the parameters of a teacher neuron. We show that complex temporal
    functions can be learned online and without backpropagation through time, relying
    on event-based updates only. Our results are a step towards online learning of
    neural computations from ungraded and unsigned sparse feedback signals with a
    biologically inspired learning mechanism."
acknowledgement: We would like to thank Professor Dr. Henning Sprekeler for his valuable
  suggestions and Dr. Andrew Saxe, Milan Klöwer and Anna Wallis for their constructive
  feedback on the manuscript. Lukas Braun was supported by the Network of European
  Neuroscience Schools through their NENS Exchange Grant program, by the European
  Union through their European Community Action Scheme for the Mobility of University
  Students, the Woodward Scholarship awarded by Wadham College, Oxford and the Medical
  Research Council [MR/N013468/1]. Tim P. Vogels was supported by a Wellcome Trust
  Senior Research Fellowship [214316/Z/18/Z].
article_processing_charge: No
author:
- first_name: Lukas
  full_name: Braun, Lukas
  last_name: Braun
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: 'Braun L, Vogels TP. Online learning of neural computations from sparse temporal
    feedback. In: <i>Advances in Neural Information Processing Systems - 35th Conference
    on Neural Information Processing Systems</i>. Vol 20. Neural Information Processing
    Systems Foundation; 2021:16437-16450.'
  apa: 'Braun, L., &#38; Vogels, T. P. (2021). Online learning of neural computations
    from sparse temporal feedback. In <i>Advances in Neural Information Processing
    Systems - 35th Conference on Neural Information Processing Systems</i> (Vol. 20,
    pp. 16437–16450). Virtual, Online: Neural Information Processing Systems Foundation.'
  chicago: Braun, Lukas, and Tim P Vogels. “Online Learning of Neural Computations
    from Sparse Temporal Feedback.” In <i>Advances in Neural Information Processing
    Systems - 35th Conference on Neural Information Processing Systems</i>, 20:16437–50.
    Neural Information Processing Systems Foundation, 2021.
  ieee: L. Braun and T. P. Vogels, “Online learning of neural computations from sparse
    temporal feedback,” in <i>Advances in Neural Information Processing Systems -
    35th Conference on Neural Information Processing Systems</i>, Virtual, Online,
    2021, vol. 20, pp. 16437–16450.
  ista: 'Braun L, Vogels TP. 2021. Online learning of neural computations from sparse
    temporal feedback. Advances in Neural Information Processing Systems - 35th Conference
    on Neural Information Processing Systems. NeurIPS: Neural Information Processing
    Systems vol. 20, 16437–16450.'
  mla: Braun, Lukas, and Tim P. Vogels. “Online Learning of Neural Computations from
    Sparse Temporal Feedback.” <i>Advances in Neural Information Processing Systems
    - 35th Conference on Neural Information Processing Systems</i>, vol. 20, Neural
    Information Processing Systems Foundation, 2021, pp. 16437–50.
  short: L. Braun, T.P. Vogels, in:, Advances in Neural Information Processing Systems
    - 35th Conference on Neural Information Processing Systems, Neural Information
    Processing Systems Foundation, 2021, pp. 16437–16450.
conference:
  end_date: 2021-12-14
  location: Virtual, Online
  name: 'NeurIPS: Neural Information Processing Systems'
  start_date: 2021-12-06
corr_author: '1'
date_created: 2022-06-19T22:01:59Z
date_published: 2021-12-01T00:00:00Z
date_updated: 2025-04-14T09:44:14Z
day: '01'
department:
- _id: TiVo
intvolume: '        20'
language:
- iso: eng
main_file_link:
- open_access: '1'
  url: https://proceedings.neurips.cc/paper/2021/file/88e1ce84f9feef5a08d0df0334c53468-Paper.pdf
month: '12'
oa: 1
oa_version: Published Version
page: 16437-16450
project:
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: "Whatâ\x80\x99s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks."
publication: Advances in Neural Information Processing Systems - 35th Conference on
  Neural Information Processing Systems
publication_identifier:
  isbn:
  - '9781713845393'
  issn:
  - 1049-5258
publication_status: published
publisher: Neural Information Processing Systems Foundation
quality_controlled: '1'
scopus_import: '1'
status: public
title: Online learning of neural computations from sparse temporal feedback
type: conference
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 20
year: '2021'
...
---
_id: '8253'
abstract:
- lang: eng
  text: Brains process information in spiking neural networks. Their intricate connections
    shape the diverse functions these networks perform. In comparison, the functional
    capabilities of models of spiking networks are still rudimentary. This shortcoming
    is mainly due to the lack of insight and practical algorithms to construct the
    necessary connectivity. Any such algorithm typically attempts to build networks
    by iteratively reducing the error compared to a desired output. But assigning
    credit to hidden units in multi-layered spiking networks has remained challenging
    due to the non-differentiable nonlinearity of spikes. To avoid this issue, one
    can employ surrogate gradients to discover the required connectivity in spiking
    network models. However, the choice of a surrogate is not unique, raising the
    question of how its implementation influences the effectiveness of the method.
    Here, we use numerical simulations to systematically study how essential design
    parameters of surrogate gradients impact learning performance on a range of classification
    problems. We show that surrogate gradient learning is robust to different shapes
    of underlying surrogate derivatives, but the choice of the derivative’s scale
    can substantially affect learning performance. When we combine surrogate gradients
    with a suitable activity regularization technique, robust information processing
    can be achieved in spiking networks even at the sparse activity limit. Our study
    provides a systematic account of the remarkable robustness of surrogate gradient
    learning and serves as a practical guide to model functional spiking neural networks.
acknowledgement: F.Z. was supported by the Wellcome Trust (110124/Z/15/Z) and the
  Novartis Research Foundation. T.P.V. was supported by a Wellcome Trust Sir Henry
  Dale Research fellowship (WT100000), a Wellcome Trust Senior Research Fellowship
  (214316/Z/18/Z), and an ERC Consolidator Grant SYNAPSEEK.
article_processing_charge: No
article_type: original
author:
- first_name: Friedemann
  full_name: Zenke, Friedemann
  last_name: Zenke
  orcid: 0000-0003-1883-644X
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: Zenke F, Vogels TP. The remarkable robustness of surrogate gradient learning
    for instilling complex function in spiking neural networks. <i>Neural Computation</i>.
    2021;33(4):899-925. doi:<a href="https://doi.org/10.1162/neco_a_01367">10.1162/neco_a_01367</a>
  apa: Zenke, F., &#38; Vogels, T. P. (2021). The remarkable robustness of surrogate
    gradient learning for instilling complex function in spiking neural networks.
    <i>Neural Computation</i>. MIT Press. <a href="https://doi.org/10.1162/neco_a_01367">https://doi.org/10.1162/neco_a_01367</a>
  chicago: Zenke, Friedemann, and Tim P Vogels. “The Remarkable Robustness of Surrogate
    Gradient Learning for Instilling Complex Function in Spiking Neural Networks.”
    <i>Neural Computation</i>. MIT Press, 2021. <a href="https://doi.org/10.1162/neco_a_01367">https://doi.org/10.1162/neco_a_01367</a>.
  ieee: F. Zenke and T. P. Vogels, “The remarkable robustness of surrogate gradient
    learning for instilling complex function in spiking neural networks,” <i>Neural
    Computation</i>, vol. 33, no. 4. MIT Press, pp. 899–925, 2021.
  ista: Zenke F, Vogels TP. 2021. The remarkable robustness of surrogate gradient
    learning for instilling complex function in spiking neural networks. Neural Computation.
    33(4), 899–925.
  mla: Zenke, Friedemann, and Tim P. Vogels. “The Remarkable Robustness of Surrogate
    Gradient Learning for Instilling Complex Function in Spiking Neural Networks.”
    <i>Neural Computation</i>, vol. 33, no. 4, MIT Press, 2021, pp. 899–925, doi:<a
    href="https://doi.org/10.1162/neco_a_01367">10.1162/neco_a_01367</a>.
  short: F. Zenke, T.P. Vogels, Neural Computation 33 (2021) 899–925.
corr_author: '1'
date_created: 2020-08-12T12:08:24Z
date_published: 2021-03-01T00:00:00Z
date_updated: 2025-04-14T09:44:14Z
day: '01'
ddc:
- '000'
- '570'
department:
- _id: TiVo
doi: 10.1162/neco_a_01367
ec_funded: 1
external_id:
  isi:
  - '000663433900003'
  pmid:
  - '33513328'
file:
- access_level: open_access
  checksum: eac5a51c24c8989ae7cf9ae32ec3bc95
  content_type: application/pdf
  creator: dernst
  date_created: 2022-04-08T06:05:39Z
  date_updated: 2022-04-08T06:05:39Z
  file_id: '11131'
  file_name: 2021_NeuralComputation_Zenke.pdf
  file_size: 1611614
  relation: main_file
  success: 1
file_date_updated: 2022-04-08T06:05:39Z
has_accepted_license: '1'
intvolume: '        33'
isi: 1
issue: '4'
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
page: 899-925
pmid: 1
project:
- _id: 0aacfa84-070f-11eb-9043-d7eb2c709234
  call_identifier: H2020
  grant_number: '819603'
  name: Learning the shape of synaptic plasticity rules for neuronal architectures
    and function through machine learning.
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: "Whatâ\x80\x99s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks."
publication: Neural Computation
publication_identifier:
  eissn:
  - 1530-888X
  issn:
  - 0899-7667
publication_status: published
publisher: MIT Press
quality_controlled: '1'
scopus_import: '1'
status: public
title: The remarkable robustness of surrogate gradient learning for instilling complex
  function in spiking neural networks
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 33
year: '2021'
...
---
_id: '9633'
abstract:
- lang: eng
  text: The search for biologically faithful synaptic plasticity rules has resulted
    in a large body of models. They are usually inspired by – and fitted to – experimental
    data, but they rarely produce neural dynamics that serve complex functions. These
    failures suggest that current plasticity models are still under-constrained by
    existing data. Here, we present an alternative approach that uses meta-learning
    to discover plausible synaptic plasticity rules. Instead of experimental data,
    the rules are constrained by the functions they implement and the structure they
    are meant to produce. Briefly, we parameterize synaptic plasticity rules by a
    Volterra expansion and then use supervised learning methods (gradient descent
    or evolutionary strategies) to minimize a problem-dependent loss function that
    quantifies how effectively a candidate plasticity rule transforms an initially
    random network into one with the desired function. We first validate our approach
    by re-discovering previously described plasticity rules, starting at the single-neuron
    level and “Oja’s rule”, a simple Hebbian plasticity rule that captures the direction
    of most variability of inputs to a neuron (i.e., the first principal component).
    We expand the problem to the network level and ask the framework to find Oja’s
    rule together with an anti-Hebbian rule such that an initially random two-layer
    firing-rate network will recover several principal components of the input space
    after learning. Next, we move to networks of integrate-and-fire neurons with plastic
    inhibitory afferents. We train for rules that achieve a target firing rate by
    countering tuned excitation. Our algorithm discovers a specific subset of the
    manifold of rules that can solve this task. Our work is a proof of principle of
    an automated and unbiased approach to unveil synaptic plasticity rules that obey
    biological constraints and can solve complex functions.
acknowledgement: We would like to thank Chaitanya Chintaluri, Georgia Christodoulou,
  Bill Podlaski and Merima Šabanovic for useful discussions and comments. This work
  was supported by a Wellcome Trust ´ Senior Research Fellowship (214316/Z/18/Z),
  a BBSRC grant (BB/N019512/1), an ERC consolidator Grant (SYNAPSEEK), a Leverhulme
  Trust Project Grant (RPG-2016-446), and funding from École Polytechnique, Paris.
article_processing_charge: No
author:
- first_name: Basile J
  full_name: Confavreux, Basile J
  id: C7610134-B532-11EA-BD9F-F5753DDC885E
  last_name: Confavreux
- first_name: Friedemann
  full_name: Zenke, Friedemann
  last_name: Zenke
- first_name: Everton J.
  full_name: Agnes, Everton J.
  last_name: Agnes
- first_name: Timothy
  full_name: Lillicrap, Timothy
  last_name: Lillicrap
- first_name: Tim P
  full_name: Vogels, Tim P
  id: CB6FF8D2-008F-11EA-8E08-2637E6697425
  last_name: Vogels
  orcid: 0000-0003-3295-6181
citation:
  ama: 'Confavreux BJ, Zenke F, Agnes EJ, Lillicrap T, Vogels TP. A meta-learning
    approach to (re)discover plasticity rules that carve a desired function into a
    neural network. In: <i>Advances in Neural Information Processing Systems</i>.
    Vol 33. ; 2020:16398-16408.'
  apa: Confavreux, B. J., Zenke, F., Agnes, E. J., Lillicrap, T., &#38; Vogels, T.
    P. (2020). A meta-learning approach to (re)discover plasticity rules that carve
    a desired function into a neural network. In <i>Advances in Neural Information
    Processing Systems</i> (Vol. 33, pp. 16398–16408). Vancouver, Canada.
  chicago: Confavreux, Basile J, Friedemann Zenke, Everton J. Agnes, Timothy Lillicrap,
    and Tim P Vogels. “A Meta-Learning Approach to (Re)Discover Plasticity Rules That
    Carve a Desired Function into a Neural Network.” In <i>Advances in Neural Information
    Processing Systems</i>, 33:16398–408, 2020.
  ieee: B. J. Confavreux, F. Zenke, E. J. Agnes, T. Lillicrap, and T. P. Vogels, “A
    meta-learning approach to (re)discover plasticity rules that carve a desired function
    into a neural network,” in <i>Advances in Neural Information Processing Systems</i>,
    Vancouver, Canada, 2020, vol. 33, pp. 16398–16408.
  ista: 'Confavreux BJ, Zenke F, Agnes EJ, Lillicrap T, Vogels TP. 2020. A meta-learning
    approach to (re)discover plasticity rules that carve a desired function into a
    neural network. Advances in Neural Information Processing Systems. NeurIPS: Conference
    on Neural Information Processing Systems vol. 33, 16398–16408.'
  mla: Confavreux, Basile J., et al. “A Meta-Learning Approach to (Re)Discover Plasticity
    Rules That Carve a Desired Function into a Neural Network.” <i>Advances in Neural
    Information Processing Systems</i>, vol. 33, 2020, pp. 16398–408.
  short: B.J. Confavreux, F. Zenke, E.J. Agnes, T. Lillicrap, T.P. Vogels, in:, Advances
    in Neural Information Processing Systems, 2020, pp. 16398–16408.
conference:
  end_date: 2020-12-12
  location: Vancouver, Canada
  name: 'NeurIPS: Conference on Neural Information Processing Systems'
  start_date: 2020-12-06
date_created: 2021-07-04T22:01:27Z
date_published: 2020-12-06T00:00:00Z
date_updated: 2026-04-27T22:30:20Z
day: '06'
department:
- _id: TiVo
ec_funded: 1
intvolume: '        33'
language:
- iso: eng
main_file_link:
- open_access: '1'
  url: https://proceedings.neurips.cc/paper/2020/hash/bdbd5ebfde4934142c8a88e7a3796cd5-Abstract.html
month: '12'
oa: 1
oa_version: Published Version
page: 16398-16408
project:
- _id: 0aacfa84-070f-11eb-9043-d7eb2c709234
  call_identifier: H2020
  grant_number: '819603'
  name: Learning the shape of synaptic plasticity rules for neuronal architectures
    and function through machine learning.
- _id: c084a126-5a5b-11eb-8a69-d75314a70a87
  grant_number: 214316/Z/18/Z
  name: What’s in a memory? Spatiotemporal dynamics in strongly coupled recurrent
    neuronal networks.
publication: Advances in Neural Information Processing Systems
publication_identifier:
  issn:
  - 1049-5258
publication_status: published
quality_controlled: '1'
related_material:
  link:
  - relation: is_continued_by
    url: https://doi.org/10.1101/2020.10.24.353409
  record:
  - id: '14422'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: A meta-learning approach to (re)discover plasticity rules that carve a desired
  function into a neural network
type: conference
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 33
year: '2020'
...
