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      Beyond spiking networks: The computational advantages of dendritic amplification and input segregation

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          Significance

          Biological networks embody the capability to flexibly support a disparate variety of functions, learning with astonishing energy and sample efficiency. This motivates the search for biologically inspired learning rules for improving artificial intelligence. We propose a generation of bio-inspired networks composed of three-compartment neurons (inspired by L5 pyramidal neurons) and a paradigm for learning and computing. This generation of networks achieves properties that are inaccessible to standard networks, among which the capability to learn without error propagation, the possibility to robustly perform context-dependent tasks, and the possibility to implement hierarchical policies decomposing complex long-horizon tasks. Finally, we argue that our model is capable of accounting for context-dependent perceptive facilitation observed in humans and animals.

          Abstract

          The brain can efficiently learn a wide range of tasks, motivating the search for biologically inspired learning rules for improving current artificial intelligence technology. Most biological models are composed of point neurons and cannot achieve state-of-the-art performance in machine learning. Recent works have proposed that input segregation (neurons receive sensory information and higher-order feedback in segregated compartments), and nonlinear dendritic computation would support error backpropagation in biological neurons. However, these approaches require propagating errors with a fine spatiotemporal structure to all the neurons, which is unlikely to be feasible in a biological network. To relax this assumption, we suggest that bursts and dendritic input segregation provide a natural support for target-based learning, which propagates targets rather than errors. A coincidence mechanism between the basal and the apical compartments allows for generating high-frequency bursts of spikes. This architecture supports a burst-dependent learning rule, based on the comparison between the target bursting activity triggered by the teaching signal and the one caused by the recurrent connections, providing support for target-based learning. We show that this framework can be used to efficiently solve spatiotemporal tasks, such as context-dependent store and recall of three-dimensional trajectories, and navigation tasks. Finally, we suggest that this neuronal architecture naturally allows for orchestrating “hierarchical imitation learning”, enabling the decomposition of challenging long-horizon decision-making tasks into simpler subtasks. We show a possible implementation of this in a two-level network, where the high network produces the contextual signal for the low network.

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          Most cited references29

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          A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex.

          A basic feature of intelligent systems such as the cerebral cortex is the ability to freely associate aspects of perceived experience with an internal representation of the world and make predictions about the future. Here, a hypothesis is presented that the extraordinary performance of the cortex derives from an associative mechanism built in at the cellular level to the basic cortical neuronal unit: the pyramidal cell. The mechanism is robustly triggered by coincident input to opposite poles of the neuron, is exquisitely matched to the large- and fine-scale architecture of the cortex, and is tightly controlled by local microcircuits of inhibitory neurons targeting subcellular compartments. This article explores the experimental evidence and the implications for how the cortex operates. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            Homeostatic plasticity in the developing nervous system.

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              Networks of spiking neurons: The third generation of neural network models

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                Author and article information

                Contributors
                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                29 November 2023
                5 December 2023
                29 May 2024
                : 120
                : 49
                : e2220743120
                Affiliations
                [1] aIstituto Nazionale di Fisica Nucleare (INFN), Sezione di Roma , Rome 00185, Italy
                [2] bScuola Internazionale Superiore di Studi Avanzati (SISSA), Visual Neuroscience Lab , Trieste 34136, Italy
                Author notes
                2To whom correspondence may be addressed. Email: cristiano0capone@ 123456gmail.com .

                Edited by Terrence Sejnowski, Salk Institute for Biological Studies, San Diego, CA; received December 7, 2022; accepted October 11, 2023

                1C.C. and C.L. contributed equally to this work.

                3Present address: National Center for Radiation Protection and Computational Physics, Istituto Superiore di Sanità, Rome 00161, Italy.

                Author information
                https://orcid.org/0000-0002-9958-2551
                https://orcid.org/0000-0002-2651-1277
                https://orcid.org/0000-0003-4520-5950
                https://orcid.org/0000-0003-1937-6086
                Article
                202220743
                10.1073/pnas.2220743120
                10710097
                38019856
                47a0a394-e024-4bb3-9441-6d1765774c85
                Copyright © 2023 the Author(s). Published by PNAS.

                This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 07 December 2022
                : 11 October 2023
                Page count
                Pages: 12, Words: 8550
                Funding
                Funded by: EC | Horizon 2020 Framework Programme (H2020), FundRef 100010661;
                Award ID: 945539
                Award Recipient : Cristiano Capone Award Recipient : Cosimo Lupo Award Recipient : Pier Stanislao Paolucci
                Funded by: EC | Horizon 2020 Framework Programme (H2020), FundRef 100010661;
                Award ID: 785907
                Award Recipient : Cristiano Capone Award Recipient : Cosimo Lupo Award Recipient : Pier Stanislao Paolucci
                Funded by: FAIR PE0000013 PNRR Project, FundRef ;
                Award ID: CUP I53C22001400006
                Award Recipient : Cosimo Lupo Award Recipient : Pier Stanislao Paolucci
                Funded by: EBRAINS-Italy IR00011 PNRR Project, FundRef ;
                Award ID: CUP B51E22000150006
                Award Recipient : Cosimo Lupo Award Recipient : Pier Stanislao Paolucci
                Categories
                research-article, Research Article
                neuro, Neuroscience
                424
                Biological Sciences
                Neuroscience

                dendritic amplification,pyramidal neuron,target-based learning,hierarchical imitation learning

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