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      Fundamental bounds on learning performance in neural circuits

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          Significance

          We show how neural circuits can use additional connectivity to achieve faster and more precise learning. Biologically, internal synaptic noise imposes an optimal size of network for learning a given task. Above the optimal size, addition of neurons and synaptic connections starts to impede learning and task performance. Overall brain size may therefore be constrained by pressure to learn effectively with unreliable synapses and may explain why certain neurological learning deficits are associated with hyperconnectivity. Beneath this optimal size, apparently redundant connections are advantageous for learning. Such apparently redundant connections have recently been observed in several species and brain areas.

          Abstract

          How does the size of a neural circuit influence its learning performance? Larger brains tend to be found in species with higher cognitive function and learning ability. Intuitively, we expect the learning capacity of a neural circuit to grow with the number of neurons and synapses. We show how adding apparently redundant neurons and connections to a network can make a task more learnable. Consequently, large neural circuits can either devote connectivity to generating complex behaviors or exploit this connectivity to achieve faster and more precise learning of simpler behaviors. However, we show that in a biologically relevant setting where synapses introduce an unavoidable amount of noise, there is an optimal size of network for a given task. Above the optimal network size, the addition of neurons and synaptic connections starts to impede learning performance. This suggests that the size of brain circuits may be constrained by the need to learn efficiently with unreliable synapses and provides a hypothesis for why some neurological learning deficits are associated with hyperconnectivity. Our analysis is independent of specific learning rules and uncovers fundamental relationships between learning rate, task performance, network size, and intrinsic noise in neural circuits.

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          Most cited references31

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          Noise in the nervous system.

          Noise--random disturbances of signals--poses a fundamental problem for information processing and affects all aspects of nervous-system function. However, the nature, amount and impact of noise in the nervous system have only recently been addressed in a quantitative manner. Experimental and computational methods have shown that multiple noise sources contribute to cellular and behavioural trial-to-trial variability. We review the sources of noise in the nervous system, from the molecular to the behavioural level, and show how noise contributes to trial-to-trial variability. We highlight how noise affects neuronal networks and the principles the nervous system applies to counter detrimental effects of noise, and briefly discuss noise's potential benefits.
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            Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats.

            The role of the cerebellar cortex in motor learning was investigated by comparing the paramedian lobule of adult rats given difficult acrobatic training to that of rats that had been given extensive physical exercise or had been inactive. The paramedian lobule is activated during limb movements used in both acrobatic training and physical exercise. Acrobatic animals had greater numbers of synapses per Purkinje cell than animals from the exercise or inactive groups. No significant difference in synapse number or size between the exercised and inactive groups was found. This indicates that motor learning required of the acrobatic animals, and not repetitive use of synapses during physical exercise, generates new synapses in cerebellar cortex. In contrast, exercise animals had a greater density of blood vessels in the molecular layer than did either the acrobatic or inactive animals, suggesting that increased synaptic activity elicited compensatory angiogenesis.
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              The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost.

              Neuroscientists have become used to a number of "facts" about the human brain: It has 100 billion neurons and 10- to 50-fold more glial cells; it is the largest-than-expected for its body among primates and mammals in general, and therefore the most cognitively able; it consumes an outstanding 20% of the total body energy budget despite representing only 2% of body mass because of an increased metabolic need of its neurons; and it is endowed with an overdeveloped cerebral cortex, the largest compared with brain size. These facts led to the widespread notion that the human brain is literally extraordinary: an outlier among mammalian brains, defying evolutionary rules that apply to other species, with a uniqueness seemingly necessary to justify the superior cognitive abilities of humans over mammals with even larger brains. These facts, with deep implications for neurophysiology and evolutionary biology, are not grounded on solid evidence or sound assumptions, however. Our recent development of a method that allows rapid and reliable quantification of the numbers of cells that compose the whole brain has provided a means to verify these facts. Here, I review this recent evidence and argue that, with 86 billion neurons and just as many nonneuronal cells, the human brain is a scaled-up primate brain in its cellular composition and metabolic cost, with a relatively enlarged cerebral cortex that does not have a relatively larger number of brain neurons yet is remarkable in its cognitive abilities and metabolism simply because of its extremely large number of neurons.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                21 May 2019
                6 May 2019
                6 May 2019
                : 116
                : 21
                : 10537-10546
                Affiliations
                [1] aDepartment of Engineering, University of Cambridge, Cambridge CB21PZ, United Kingdom
                Author notes
                1To whom correspondence may be addressed. Email: tso24@ 123456cam.ac.uk or dvr23@ 123456cam.ac.uk .

                Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved March 4, 2019 (received for review August 3, 2018)

                Author contributions: D.V.R. and T.O. designed research; D.V.R. and A.P.R. performed research; D.V.R., A.P.R., and T.O. analyzed data; D.V.R. and T.O. wrote the paper; and T.O. interpreted results.

                Author information
                http://orcid.org/0000-0002-8992-1353
                http://orcid.org/0000-0002-1029-0158
                Article
                201813416
                10.1073/pnas.1813416116
                6535002
                31061133
                4e31fc5d-0498-4d7e-94eb-848a735933a6
                Copyright © 2019 the Author(s). Published by PNAS.

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

                History
                Page count
                Pages: 10
                Funding
                Funded by: EC | H2020 | H2020 Priority Excellent Science | H2020 European Research Council (ERC) 100010663
                Award ID: StG-2016 FLEXNEURO (716643)
                Award Recipient : Dhruva Venkita Raman Award Recipient : Adriana Perez-Rotondo Award Recipient : Timothy OʾLeary
                Categories
                PNAS Plus
                Biological Sciences
                Neuroscience
                PNAS Plus

                learning,neural network,synaptic plasticity,optimization,artificial intelligence

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