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      Attention stabilizes the shared gain of V4 populations

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          Abstract

          Responses of sensory neurons represent stimulus information, but are also influenced by internal state. For example, when monkeys direct their attention to a visual stimulus, the response gain of specific subsets of neurons in visual cortex changes. Here, we develop a functional model of population activity to investigate the structure of this effect. We fit the model to the spiking activity of bilateral neural populations in area V4, recorded while the animal performed a stimulus discrimination task under spatial attention. The model reveals four separate time-varying shared modulatory signals, the dominant two of which each target task-relevant neurons in one hemisphere. In attention-directed conditions, the associated shared modulatory signal decreases in variance. This finding provides an interpretable and parsimonious explanation for previous observations that attention reduces variability and noise correlations of sensory neurons. Finally, the recovered modulatory signals reflect previous reward, and are predictive of subsequent choice behavior.

          DOI: http://dx.doi.org/10.7554/eLife.08998.001

          eLife digest

          Our brains receive an enormous amount of information from our senses. However, we can’t deal with it all at once; the brain must selectively focus on a portion of this information. This process of selective focus is generally called “attention”. In the visual system, this is believed to operate as a kind of amplifier that selectively boosts the signals of a particular subset of nerve cells (also known as “neurons”).

          Rabinowitz et al. built a model to study the activity of large populations of neurons in an area of the visual cortex known as V4. This model made it possible to detect hidden signals that control the attentional boosting of these neurons. Rabinowitz et al. show that when a monkey carries out a visual task, the neurons in V4 are under the influence of a small number of shared amplification signals that fluctuate in strength. These amplification signals selectively affect V4 neurons that process different parts of the visual scene. Furthermore, when the monkey directs their attention to a part of the visual scene, the associated amplifier reduces its fluctuations. This has the side effect of both boosting and stabilizing the responses of the affected V4 neurons, as well as increasing their independence.

          Rabinowitz et al.’s findings suggest that when we focus our attention on incoming information, we make the responses of particular neurons larger and reduce unwanted variability to improve the quality of the represented information. The next challenge is to understand what causes these fluctuations in the amplification signals.

          DOI: http://dx.doi.org/10.7554/eLife.08998.002

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          Most cited references70

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          Spatio-temporal correlations and visual signalling in a complete neuronal population.

          Statistical dependencies in the responses of sensory neurons govern both the amount of stimulus information conveyed and the means by which downstream neurons can extract it. Although a variety of measurements indicate the existence of such dependencies, their origin and importance for neural coding are poorly understood. Here we analyse the functional significance of correlated firing in a complete population of macaque parasol retinal ganglion cells using a model of multi-neuron spike responses. The model, with parameters fit directly to physiological data, simultaneously captures both the stimulus dependence and detailed spatio-temporal correlations in population responses, and provides two insights into the structure of the neural code. First, neural encoding at the population level is less noisy than one would expect from the variability of individual neurons: spike times are more precise, and can be predicted more accurately when the spiking of neighbouring neurons is taken into account. Second, correlations provide additional sensory information: optimal, model-based decoding that exploits the response correlation structure extracts 20% more information about the visual scene than decoding under the assumption of independence, and preserves 40% more visual information than optimal linear decoding. This model-based approach reveals the role of correlated activity in the retinal coding of visual stimuli, and provides a general framework for understanding the importance of correlated activity in populations of neurons.
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            The variable discharge of cortical neurons: implications for connectivity, computation, and information coding.

            Cortical neurons exhibit tremendous variability in the number and temporal distribution of spikes in their discharge patterns. Furthermore, this variability appears to be conserved over large regions of the cerebral cortex, suggesting that it is neither reduced nor expanded from stage to stage within a processing pathway. To investigate the principles underlying such statistical homogeneity, we have analyzed a model of synaptic integration incorporating a highly simplified integrate and fire mechanism with decay. We analyzed a "high-input regime" in which neurons receive hundreds of excitatory synaptic inputs during each interspike interval. To produce a graded response in this regime, the neuron must balance excitation with inhibition. We find that a simple integrate and fire mechanism with balanced excitation and inhibition produces a highly variable interspike interval, consistent with experimental data. Detailed information about the temporal pattern of synaptic inputs cannot be recovered from the pattern of output spikes, and we infer that cortical neurons are unlikely to transmit information in the temporal pattern of spike discharge. Rather, we suggest that quantities are represented as rate codes in ensembles of 50-100 neurons. These column-like ensembles tolerate large fractions of common synaptic input and yet covary only weakly in their spike discharge. We find that an ensemble of 100 neurons provides a reliable estimate of rate in just one interspike interval (10-50 msec). Finally, we derived an expression for the variance of the neural spike count that leads to a stable propagation of signal and noise in networks of neurons-that is, conditions that do not impose an accumulation or diminution of noise. The solution implies that single neurons perform simple algebra resembling averaging, and that more sophisticated computations arise by virtue of the anatomical convergence of novel combinations of inputs to the cortical column from external sources.
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              Attention improves performance primarily by reducing interneuronal correlations

              Visual attention can dramatically improve behavioural performance by allowing observers to focus on the important information in a complex scene. Attention also typically increases the firing rates of cortical sensory neurons. Rate increases improve the signal-to-noise ratio of individual neurons, and this improvement has been assumed to underlie attention-related improvements in behaviour. We recorded dozens of neurons simultaneously in visual area V4 and found that changes in single neurons accounted for only a small fraction of the improvement in the sensitivity of the population. Instead, over 80% of the attentional improvement in the population signal was caused by decreases in the correlations between the trial-to-trial fluctuations in the responses of pairs of neurons. These results suggest that the representation of sensory information in populations of neurons and the way attention affects the sensitivity of the population may only be understood by considering the interactions between neurons.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                02 November 2015
                2015
                : 4
                : e08998
                Affiliations
                [1 ]deptCenter for Neural Science , Howard Hughes Medical Institute, New York University , New York, United States
                [2 ]deptDepartment of Neuroscience and Center for the Neural Basis of Cognition , University of Pittsburgh , Pittsburgh, United States
                [3]University College London , United Kingdom
                [4]University College London , United Kingdom
                Author notes
                Article
                08998
                10.7554/eLife.08998
                4758958
                26523390
                a49c8484-7103-404d-83e6-e3a6d46afe7c
                © 2015, Rabinowitz 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
                : 26 May 2015
                : 01 November 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 4R00EY020844-03
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01 EY022930
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100006211, Klingenstein Third Generation Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Award ID: Research Fellowship
                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
                Computational and Systems Biology
                Neuroscience
                Custom metadata
                2.5
                Populations of neurons in the macaque visual cortex are subject to shared fluctuations in gain; these signals exhibit anatomical and functional structure, and their variability is diminished under attention.

                Life sciences
                computation,sensory,vision,statistic,attention,other
                Life sciences
                computation, sensory, vision, statistic, attention, other

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