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      Circular analysis in systems neuroscience: the dangers of double dipping

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          Abstract

          A neuroscientific experiment typically generates a large amount of data, of which only a small fraction is analyzed in detail and presented in a publication. However, selection among noisy measurements can render circular an otherwise appropriate analysis and invalidate results. Here we argue that systems neuroscience needs to adjust some widespread practices to avoid the circularity that can arise from selection. In particular, 'double dipping', the use of the same dataset for selection and selective analysis, will give distorted descriptive statistics and invalid statistical inference whenever the results statistics are not inherently independent of the selection criteria under the null hypothesis. To demonstrate the problem, we apply widely used analyses to noise data known to not contain the experimental effects in question. Spurious effects can appear in the context of both univariate activation analysis and multivariate pattern-information analysis. We suggest a policy for avoiding circularity.

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          Most cited references20

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          Distributed and overlapping representations of faces and objects in ventral temporal cortex.

          The functional architecture of the object vision pathway in the human brain was investigated using functional magnetic resonance imaging to measure patterns of response in ventral temporal cortex while subjects viewed faces, cats, five categories of man-made objects, and nonsense pictures. A distinct pattern of response was found for each stimulus category. The distinctiveness of the response to a given category was not due simply to the regions that responded maximally to that category, because the category being viewed also could be identified on the basis of the pattern of response when those regions were excluded from the analysis. Patterns of response that discriminated among all categories were found even within cortical regions that responded maximally to only one category. These results indicate that the representations of faces and objects in ventral temporal cortex are widely distributed and overlapping.
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            Information-based functional brain mapping.

            The development of high-resolution neuroimaging and multielectrode electrophysiological recording provides neuroscientists with huge amounts of multivariate data. The complexity of the data creates a need for statistical summary, but the local averaging standardly applied to this end may obscure the effects of greatest neuroscientific interest. In neuroimaging, for example, brain mapping analysis has focused on the discovery of activation, i.e., of extended brain regions whose average activity changes across experimental conditions. Here we propose to ask a more general question of the data: Where in the brain does the activity pattern contain information about the experimental condition? To address this question, we propose scanning the imaged volume with a "searchlight," whose contents are analyzed multivariately at each location in the brain.
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              Thresholding of statistical maps in functional neuroimaging using the false discovery rate.

              Finding objective and effective thresholds for voxelwise statistics derived from neuroimaging data has been a long-standing problem. With at least one test performed for every voxel in an image, some correction of the thresholds is needed to control the error rates, but standard procedures for multiple hypothesis testing (e.g., Bonferroni) tend to not be sensitive enough to be useful in this context. This paper introduces to the neuroscience literature statistical procedures for controlling the false discovery rate (FDR). Recent theoretical work in statistics suggests that FDR-controlling procedures will be effective for the analysis of neuroimaging data. These procedures operate simultaneously on all voxelwise test statistics to determine which tests should be considered statistically significant. The innovation of the procedures is that they control the expected proportion of the rejected hypotheses that are falsely rejected. We demonstrate this approach using both simulations and functional magnetic resonance imaging data from two simple experiments. (C)2002 Elsevier Science (USA).
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                Author and article information

                Journal
                Nature Neuroscience
                Nat Neurosci
                Springer Science and Business Media LLC
                1097-6256
                1546-1726
                May 2009
                April 26 2009
                May 2009
                : 12
                : 5
                : 535-540
                Article
                10.1038/nn.2303
                2841687
                19396166
                f56b4b50-1c5c-4733-9f4f-d4daa2514ca3
                © 2009

                http://www.springer.com/tdm

                http://www.springer.com/tdm

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