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      A common goodness-of-fit framework for neural population models using marked point process time-rescaling

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          Abstract

          A critical component of any statistical modeling procedure is the ability to assess the goodness-of-fit between a model and observed data. For spike train models of individual neurons, many goodness-of-fit measures rely on the time-rescaling theorem and assess model quality using rescaled spike times. Recently, there has been increasing interest in statistical models that describe the simultaneous spiking activity of neuron populations, either in a single brain region or across brain regions. Classically, such models have used spike sorted data to describe relationships between the identified neurons, but more recently clusterless modeling methods have been used to describe population activity using a single model. Here we develop a generalization of the time-rescaling theorem that enables comprehensive goodness-of-fit analysis for either of these classes of population models. We use the theory of marked point processes to model population spiking activity, and show that under the correct model, each spike can be rescaled individually to generate a uniformly distributed set of events in time and the space of spike marks. After rescaling, multiple well-established goodness-of-fit procedures and statistical tests are available. We demonstrate the application of these methods both to simulated data and real population spiking in rat hippocampus. We have made the MATLAB and Python code used for the analyses in this paper publicly available through our Github repository at https://github.com/Eden-Kramer-Lab/popTRT.

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          Most cited references33

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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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            Neuronal population coding of movement direction.

            Although individual neurons in the arm area of the primate motor cortex are only broadly tuned to a particular direction in three-dimensional space, the animal can very precisely control the movement of its arm. The direction of movement was found to be uniquely predicted by the action of a population of motor cortical neurons. When individual cells were represented as vectors that make weighted contributions along the axis of their preferred direction (according to changes in their activity during the movement under consideration) the resulting vector sum of all cell vectors (population vector) was in a direction congruent with the direction of movement. This population vector can be monitored during various tasks, and similar measures in other neuronal populations could be of heuristic value where there is a neural representation of variables with vectorial attributes.
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              A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects.

              Multiple factors simultaneously affect the spiking activity of individual neurons. Determining the effects and relative importance of these factors is a challenging problem in neurophysiology. We propose a statistical framework based on the point process likelihood function to relate a neuron's spiking probability to three typical covariates: the neuron's own spiking history, concurrent ensemble activity, and extrinsic covariates such as stimuli or behavior. The framework uses parametric models of the conditional intensity function to define a neuron's spiking probability in terms of the covariates. The discrete time likelihood function for point processes is used to carry out model fitting and model analysis. We show that, by modeling the logarithm of the conditional intensity function as a linear combination of functions of the covariates, the discrete time point process likelihood function is readily analyzed in the generalized linear model (GLM) framework. We illustrate our approach for both GLM and non-GLM likelihood functions using simulated data and multivariate single-unit activity data simultaneously recorded from the motor cortex of a monkey performing a visuomotor pursuit-tracking task. The point process framework provides a flexible, computationally efficient approach for maximum likelihood estimation, goodness-of-fit assessment, residual analysis, model selection, and neural decoding. The framework thus allows for the formulation and analysis of point process models of neural spiking activity that readily capture the simultaneous effects of multiple covariates and enables the assessment of their relative importance.
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                Author and article information

                Contributors
                (617) 353-5288 , longtao2@bu.edu
                Journal
                J Comput Neurosci
                J Comput Neurosci
                Journal of Computational Neuroscience
                Springer US (New York )
                0929-5313
                1573-6873
                8 October 2018
                8 October 2018
                2018
                : 45
                : 2
                : 147-162
                Affiliations
                ISNI 0000 0004 1936 7558, GRID grid.189504.1, Boston University College of Arts and Sciences, ; 111 Cummington Mall, Boston, MA 02215 USA
                Author notes

                Action Editor: Byron Yu

                Article
                698
                10.1007/s10827-018-0698-4
                6208891
                30298220
                b267b73e-85f8-40a1-a62c-7d6e8ebce2f5
                © The Author(s) 2018

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 5 January 2018
                : 16 September 2018
                : 26 September 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: MH105174
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: NS094288
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: 542971
                Award Recipient :
                Categories
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                © Springer Science+Business Media, LLC, part of Springer Nature 2018

                Neurosciences
                neural modeling,neural population activity,spike trains,goodness-of-fit,time-rescaling,ks plots

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