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      Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory

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      Nature neuroscience

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          Abstract

          Selective attention filters information to limit what is encoded and maintained in working memory. Although the prefrontal cortex (PFC) is central to both selective attention and working memory, the underlying neural processes that link these cognitive abilities remain elusive. Using functional magnetic resonance imaging to guide repetitive transcranial magnetic stimulation with electroencephalographic recordings in humans, we perturbed PFC function at the inferior frontal junction prior to participants performing a selective-attention, delayed-recognition task. This resulted in diminished top-down modulation of activity in posterior cortex during early encoding stages, which predicted a subsequent decrement in working memory accuracy. Participants with stronger fronto-posterior functional connectivity displayed greater disruptive effects. Data further suggested that broad alpha band (7–14 Hz) phase coherence subserved this long distance top-down modulation. The results establish top-down modulation mediated by the prefrontal cortex as a causal link between early attentional processes and subsequent memory performance.

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          Most cited references38

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          Visual search and stimulus similarity.

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            Measuring functional connectivity during distinct stages of a cognitive task.

            The inherently multivariate nature of functional brain imaging data affords the unique opportunity to explore how anatomically disparate brain areas interact during cognitive tasks. We introduce a new method for characterizing inter-regional interactions using event-related functional magnetic resonance imaging (fMRI) data. This method's principle advantage over existing analytical techniques is its ability to model the functional connectivity between brain regions during distinct stages of a cognitive task. The method is implemented by using separate covariates to model the activity evoked during each stage of each individual trial in the context of the general linear model (GLM). The resulting parameter estimates (beta values) are sorted according to the stage from which they were derived to form a set of stage-specific beta series. Regions whose beta series are correlated during a given stage are inferred to be functionally interacting during that stage. To validate the assumption that correlated fluctuations in trial-to-trial beta values imply functional connectivity, we applied the method to an event-related fMRI data set in which subjects performed two sequence-tapping tasks. In concordance with previous electrophysiological and fMRI coherence studies, we found that the task requiring greater bimanual coordination induced stronger correlations between motor regions of the two hemispheres. The method was then applied to an event-related fMRI data set in which subjects performed a delayed recognition task. Distinct functional connectivity maps were generated during the component stages of this task, illustrating how important and novel observations of neural networks within the isolated stages of a cognitive task can be obtained.
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              A direct demonstration of functional specialization in human visual cortex.

              We have used positron emission tomography (PET), which measures regional cerebral blood flow (rCBF), to demonstrate directly the specialization of function in the normal human visual cortex. A novel technique, statistical parametric mapping, was used to detect foci of significant change in cerebral blood flow within the prestriate cortex, in order to localize those parts involved in the perception of color and visual motion. For color, we stimulated the subjects with a multicolored abstract display containing no recognizable objects (Land color Mondrian) and contrasted the resulting blood flow maps with those obtained when subjects viewed an identical display consisting of equiluminous shades of gray. The comparison identified a unique area (area V4) located in the lingual and fusiform gyri of the prestriate cortex. For motion, blood flow maps when subjects viewed moving or stationary black and white random-square patterns were contrasted. The comparison identified a unique area located in the region of the temporo-parieto-occipital junction (area V5). We thus provide direct evidence to show that, just as in the macaque monkey, different areas of the human prestriate visual cortex are specialized for different attributes of vision. The striate cortex (V1) and the contiguous visual area (V2), which in the monkey brain feed both the homologous areas, were active in all 4 conditions. This pattern of activity allowed us to use an extension of the approach to assess the functional relationship between the 3 areas during color and motion stimulation. This is based on an hypothesis-led analysis of the covariance structure of the blood flow maps and promises to be a powerful tool for inferring anatomical pathways in the normal human brain.(ABSTRACT TRUNCATED AT 250 WORDS)
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                24 February 2011
                27 March 2011
                May 2011
                1 November 2011
                : 14
                : 5
                : 656-661
                Author notes

                Author Contributions T.P.Z., A.T., and A.G. conceptualized and designed the task. T.P.Z. and M.T.R. performed the experiment. T.P.Z. analyzed the data. T.P.Z. and A.G. wrote the paper.

                Corresponding author: Theodore Zanto UCSF – MC2240 600 16 th St., Genentech Hall Room N474 San Francisco, CA 94158 Tel: 1-415-476-2164 Fax: 1-415-502-1655 theodore.zanto@ 123456ucsf.edu
                Article
                nihpa271132
                10.1038/nn.2773
                3083493
                21441920
                f3e7a36c-a2c7-4e1a-91d5-522f1ffe21fb

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                History
                Funding
                Funded by: National Institute on Aging : NIA
                Award ID: R01 AG030395-05 ||AG
                Funded by: National Institute on Aging : NIA
                Award ID: F32 AG030249-01A2 ||AG
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                Neurosciences
                Neurosciences

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