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      Decoding of Repeated Objects from Local Field Potentials in Macaque Inferior Temporal Cortex

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      PLoS ONE
      Public Library of Science

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          Abstract

          Stimulus repetition produces a decrease of the response and affects neuronal synchronization of macaque inferior temporal (IT) neurons. Previously we showed that such stimulus-specific adaptation results in a decreased accuracy by which IT neurons encode repeated compared to non-repeated objects. Not only spiking activity, but also local field potentials (LFPs) are affected by repetition. Here we ask how the repetition-induced changes in IT LFPs affect object decoding accuracy. To answer this, we recorded local field potentials using a laminar microelectrode in macaque IT. We presented two familiar stimuli each for 500 ms successively with an inter-stimulus interval of 500 ms. Trials consisted either of a repetition of the same stimulus or of their alternation. Machine learning-based classifier was employed to decode stimulus identity from the LFP power in different frequency bands of each penetration. We found that the object classification accuracy depended strongly on spectral frequency, with frequencies below 30 Hz (alpha and beta) producing greater accuracies than gamma bands. However, the effect of repetition on classification accuracy was stronger at the gamma frequencies, showing a decrease in classification accuracy for repeated stimuli and a tendency for an improved object encoding when the stimulus was preceded by a different stimulus. The present results demonstrate that due to adapting input, stimulus encoding in IT (1) can be more accurate for stimuli that differ from recently preceding ones while being impaired for stimuli that are repeated, and (2) these effects are more pronounced at high spectral frequencies of the LFP.

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          Most cited references45

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          Repetition and the brain: neural models of stimulus-specific effects.

          One of the most robust experience-related cortical dynamics is reduced neural activity when stimuli are repeated. This reduction has been linked to performance improvements due to repetition and also used to probe functional characteristics of neural populations. However, the underlying neural mechanisms are as yet unknown. Here, we consider three models that have been proposed to account for repetition-related reductions in neural activity, and evaluate them in terms of their ability to account for the main properties of this phenomenon as measured with single-cell recordings and neuroimaging techniques. We also discuss future directions for distinguishing between these models, which will be important for understanding the neural consequences of repetition and for interpreting repetition-related effects in neuroimaging data.
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            Temporal structure in neuronal activity during working memory in macaque parietal cortex.

            Many cortical structures have elevated firing rates during working memory, but it is not known how the activity is maintained. To investigate whether reverberating activity is important, we studied the temporal structure of local field potential (LFP) activity and spiking from area LIP in two awake macaques during a memory-saccade task. Using spectral analysis, we found spatially tuned elevated power in the gamma band (25-90 Hz) in LFP and spiking activity during the memory period. Spiking and LFP activity were also coherent in the gamma band but not at lower frequencies. Finally, we decoded LFP activity on a single-trial basis and found that LFP activity in parietal cortex discriminated between preferred and anti-preferred direction with approximately the same accuracy as the spike rate and predicted the time of a planned movement with better accuracy than the spike rate. This finding could accelerate the development of a cortical neural prosthesis.
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              Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex.

              Functional magnetic resonance imaging (fMRI) is an important tool for investigating human brain function, but the relationship between the hemodynamically based fMRI signals in the human brain and the underlying neuronal activity is unclear. We recorded single unit activity and local field potentials in auditory cortex of two neurosurgical patients and compared them with the fMRI signals of 11 healthy subjects during presentation of an identical movie segment. The predicted fMRI signals derived from single units and the measured fMRI signals from auditory cortex showed a highly significant correlation (r = 0.75, P < 10(-47)). Thus, fMRI signals can provide a reliable measure of the firing rate of human cortical neurons.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                5 September 2013
                : 8
                : 9
                : e74665
                Affiliations
                [1]Laboratorium voor Neuro- en Psychofysiologie, KU Leuven Medical School, Leuven, Belgium
                National Institute of Mental Health, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DAK RV. Performed the experiments: DAK. Analyzed the data: DAK RV. Contributed reagents/materials/analysis tools: DAK. Wrote the manuscript: DAK RV.

                Article
                PONE-D-13-17011
                10.1371/journal.pone.0074665
                3764032
                24040313
                f6f74753-c672-455c-8ffa-a42f3d85fb9e
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 April 2013
                : 4 August 2013
                Funding
                This work was supported by Fonds voor Wetenschappelijk Onderzoek Vlaanderen, Geconcerteerde Onderzoeksactie (GOA/10/019), Interuniversitaire Attractiepool and Programma Financiering (PF 10/008). For the computation of classifiers we used the infrastructure of the VSC – Flemish Supercomputer Center, funded by the Hercules Foundation and the Flemish Government – department EWI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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