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      A thesaurus for a neural population code

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          Abstract

          Information is carried in the brain by the joint spiking patterns of large groups of noisy, unreliable neurons. This noise limits the capacity of the neural code and determines how information can be transmitted and read-out. To accurately decode, the brain must overcome this noise and identify which patterns are semantically similar. We use models of network encoding noise to learn a thesaurus for populations of neurons in the vertebrate retina responding to artificial and natural videos, measuring the similarity between population responses to visual stimuli based on the information they carry. This thesaurus reveals that the code is organized in clusters of synonymous activity patterns that are similar in meaning but may differ considerably in their structure. This organization is highly reminiscent of the design of engineered codes. We suggest that the brain may use this structure and show how it allows accurate decoding of novel stimuli from novel spiking patterns.

          DOI: http://dx.doi.org/10.7554/eLife.06134.001

          eLife digest

          Our ability to perceive the world is dependent on information from our senses being passed between different parts of the brain. The information is encoded as patterns of electrical pulses or ‘spikes’, which other brain regions must be able to decipher. Cracking this code would thus enable us to predict the patterns of nerve impulses that would occur in response to specific stimuli, and ‘decode’ which stimuli had produced particular patterns of impulses.

          This task is challenging in part because of its scale—vast numbers of stimuli are encoded by huge numbers of neurons that can send their spikes in many different combinations. Furthermore, neurons are inherently noisy and their response to identical stimuli may vary considerably in the number of spikes and their timing. This means that the brain cannot simply link a single unchanging pattern of firing with each stimulus, because these firing patterns are often distorted by biophysical noise.

          Ganmor et al. have now modeled the effects of noise in a network of neurons in the retina (found at the back of the eye), and, in doing so, have provided insights into how the brain solves this problem. This has brought us a step closer to cracking the neural code. First, 10 second video clips of natural scenes and artificial stimuli were played on a loop to a sample of retina taken from a salamander, and the responses of nearly 100 neurons in the sample were recorded for two hours. Dividing the 10 second clip into short segments provided a series of 500 stimuli, which the network had been exposed to more than 600 times.

          Ganmor et al. analyzed the responses of groups of 20 cells to each stimulus and found that physically similar firing patterns were not particularly likely to encode the same stimulus. This can be likened to the way that words such as ‘light’ and ‘night’ have similar structures but different meanings. Instead, the model reveals that each stimulus was represented by a cluster of firing patterns that bore little physical resemblance to one another, but which nevertheless conveyed the same meaning. To continue on with the previous example, this is similar to way that ‘light’ and ‘illumination’ have the same meaning but different structures.

          Ganmor et al. use these new data to map the organization of the ‘vocabulary’ of populations of cells the retina, and put together a kind of ‘thesaurus’ that enables new activity patterns of the retina to be decoded and could be used to crack the neural code. Furthermore, the organization of ‘synonyms’ is strikingly similar to codes that are favored in many forms of telecommunication. In these man-made codes, codewords that represent different items are chosen to be so distinct from each other that even if they were corrupted by noise, they could be correctly deciphered. Correspondingly, in the retina, patterns that carry the same meaning occupy a distinct area, and new patterns can be interpreted based on their proximity to these clusters.

          DOI: http://dx.doi.org/10.7554/eLife.06134.002

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          Most cited references66

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          Neural networks and physical systems with emergent collective computational abilities.

          J Hopfield (1982)
          Computational properties of use of biological organisms or to the construction of computers can emerge as collective properties of systems having a large number of simple equivalent components (or neurons). The physical meaning of content-addressable memory is described by an appropriate phase space flow of the state of a system. A model of such a system is given, based on aspects of neurobiology but readily adapted to integrated circuits. The collective properties of this model produce a content-addressable memory which correctly yields an entire memory from any subpart of sufficient size. The algorithm for the time evolution of the state of the system is based on asynchronous parallel processing. Additional emergent collective properties include some capacity for generalization, familiarity recognition, categorization, error correction, and time sequence retention. The collective properties are only weakly sensitive to details of the modeling or the failure of individual devices.
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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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              Neural correlations, population coding and computation.

              How the brain encodes information in population activity, and how it combines and manipulates that activity as it carries out computations, are questions that lie at the heart of systems neuroscience. During the past decade, with the advent of multi-electrode recording and improved theoretical models, these questions have begun to yield answers. However, a complete understanding of neuronal variability, and, in particular, how it affects population codes, is missing. This is because variability in the brain is typically correlated, and although the exact effects of these correlations are not known, it is known that they can be large. Here, we review studies that address the interaction between neuronal noise and population codes, and discuss their implications for population coding in general.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                08 September 2015
                2015
                : 4
                : e06134
                Affiliations
                [1 ]deptDepartment of Neurobiology , Weizmann Institute of Science , Rehovot, Israel
                [2 ]deptDepartment of Life Sciences, Zlotowski Center for Neuroscience , Ben-Gurion University of the Negev , Beer-Sheva, Israel
                University of California, San Diego , United States
                Author notes
                Article
                06134
                10.7554/eLife.06134
                4562117
                26347983
                5ec3ba45-f8d9-4420-be3b-c7afdaeaca73
                © 2015, Ganmor et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 22 December 2014
                : 02 August 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council (ERC);
                Award ID: 311238 NEURO-POPCODE
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003977, Israel Science Foundation (ISF);
                Award ID: 1629/12
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001742, United States-Israel Binational Science Foundation (BSF);
                Award ID: 2011058
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003977, Israel Science Foundation (ISF);
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007028, Leona M. and Harry B. Helmsley Charitable Trust;
                Award ID: Ben-Gurion University
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001735, Weizmann Institute of Science;
                Award ID: Mr. Martin Kushner Schnur, Mexico
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001735, Weizmann Institute of Science;
                Award ID: Mr. and Mrs. Lawrence Feis, Winetka, IL, USA
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                2.3
                The activity patterns of populations of neurons in the retina are organized as semantic clusters (analogous to synonyms), in which component patterns bear little physical resemblance to one another but convey the same meaning.

                Life sciences
                neural code,information,noise,entropy,natural stimuli,metric,retina,salamander
                Life sciences
                neural code, information, noise, entropy, natural stimuli, metric, retina, salamander

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