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      Neural constraints on learning

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          Abstract

          Motor, sensory, and cognitive learning require networks of neurons to generate new activity patterns. Because some behaviors are easier to learn than others 1, 2 , we wondered if some neural activity patterns are easier to generate than others. We asked whether the existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define the constraint. We employed a closed-loop intracortical brain-computer interface (BCI) learning paradigm in which Rhesus monkeys controlled a computer cursor by modulating neural activity patterns in primary motor cortex. Using the BCI paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. These patterns comprise a low-dimensional space (termed the intrinsic manifold, or IM) within the high-dimensional neural firing rate space. They presumably reflect constraints imposed by the underlying neural circuitry. We found that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the IM. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the IM. This result suggests that the existing structure of a network can shape learning. On the timescale of hours, it appears to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess 3, 4 .

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          Most cited references42

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          Neural population dynamics during reaching

          Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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            Dimensionality reduction for large-scale neural recordings.

            Most sensory, cognitive and motor functions depend on the interactions of many neurons. In recent years, there has been rapid development and increasing use of technologies for recording from large numbers of neurons, either sequentially or simultaneously. A key question is what scientific insight can be gained by studying a population of recorded neurons beyond studying each neuron individually. Here, we examine three important motivations for population studies: single-trial hypotheses requiring statistical power, hypotheses of population response structure and exploratory analyses of large data sets. Many recent studies have adopted dimensionality reduction to analyze these populations and to find features that are not apparent at the level of individual neurons. We describe the dimensionality reduction methods commonly applied to population activity and offer practical advice about selecting methods and interpreting their outputs. This review is intended for experimental and computational researchers who seek to understand the role dimensionality reduction has had and can have in systems neuroscience, and who seek to apply these methods to their own data.
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              Learning-induced LTP in neocortex.

              The hypothesis that learning occurs through long-term potentiation (LTP)- and long-term depression (LTD)-like mechanisms is widely held but unproven. This hypothesis makes three assumptions: Synapses are modifiable, they modify with learning, and they strengthen through an LTP-like mechanism. We previously established the ability for synaptic modification and a synaptic strengthening with motor skill learning in horizontal connections of the rat motor cortex (MI). Here we investigated whether learning strengthened these connections through LTP. We demonstrated that synapses in the trained MI were near the ceiling of their modification range, compared with the untrained MI, but the range of synaptic modification was not affected by learning. In the trained MI, LTP was markedly reduced and LTD was enhanced. These results are consistent with the use of LTP to strengthen synapses during learning.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                15 July 2014
                28 August 2014
                11 April 2015
                : 512
                : 7515
                : 423-426
                Affiliations
                [1 ]Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America, 15261
                [2 ]Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania, United States of America, 15213
                [3 ]Department of Electrical and Computer Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America, 15213
                [4 ]Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania, United States of America, 15213
                [5 ]Department of Electrical Engineering, Stanford University, Stanford, California, United States of America, 94305
                [6 ]Department of Neurosurgery, Palo Alto Medical Foundation, Palo Alto, California, United States of America, 94301
                [7 ]Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America, 15213
                [8 ]Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America, 15213
                Author notes
                Correspondence and requests for materials should be addressed to B.M.Y. ( byronyu@ 123456cmu.edu ) or A.P.B. ( apb10@ 123456pitt.edu )
                [*]

                contributed equally

                Article
                NIHMS611861
                10.1038/nature13665
                4393644
                25164754
                b64ec1d2-9c69-45e3-9bfa-e5c863025372
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