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      Estradiol modulates neural response to conspecific and heterospecific song in female house sparrows: An in vivo positron emission tomography study

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          Abstract

          Although there is growing evidence that estradiol modulates female perception of male sexual signals, relatively little research has focused on female auditory processing. We used in vivo 18F-fluorodeoxyglucose ( 18F-FDG) positron emission tomography (PET) imaging to examine the neuronal effects of estradiol and conspecific song in female house sparrows ( Passer domesticus). We assessed brain glucose metabolism, a measure of neuronal activity, in females with empty implants, estradiol implants, and empty implants ~1 month after estradiol implant removal. Females were exposed to conspecific or heterospecific songs immediately prior to imaging. The activity of brain regions involved in auditory perception did not differ between females with empty implants exposed to conspecific vs. heterospecific song, but neuronal activity was significantly reduced in females with estradiol implants exposed to heterospecific song. Furthermore, our within-individual design revealed that changes in brain activity due to high estradiol were actually greater several weeks after peak hormone exposure. Overall, this study demonstrates that PET imaging is a powerful tool for assessing large-scale changes in brain activity in living songbirds, and suggests that after breeding is done, specific environmental and physiological cues are necessary for estradiol-stimulated females to lose the selectivity they display in neural response to conspecific song.

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          Most cited references36

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          Method for transforming CT images for attenuation correction in PET/CT imaging.

          A tube-voltage-dependent scheme is presented for transforming Hounsfield units (HU) measured by different computed tomography (CT) scanners at different x-ray tube voltages (kVp) to 511 keV linear attenuation values for attenuation correction in positron emission tomography (PET) data reconstruction. A Gammex 467 electron density CT phantom was imaged using a Siemens Sensation 16-slice CT, a Siemens Emotion 6-slice CT, a GE Lightspeed 16-slice CT, a Hitachi CXR 4-slice CT, and a Toshiba Aquilion 16-slice CT at kVp ranging from 80 to 140 kVp. All of these CT scanners are also available in combination with a PET scanner as a PET/CT tomograph. HU obtained for various reference tissue substitutes in the phantom were compared with the known linear attenuation values at 511 keV. The transformation, appropriate for lung, soft tissue, and bone, yields the function 9.6 x 10(-5). (HU+ 1000) below a threshold of approximately 50 HU and a (HU+ 1000)+b above the threshold, where a and b are fixed parameters that depend on the kVp setting. The use of the kVp-dependent scaling procedure leads to a significant improvement in reconstructed PET activity levels in phantom measurements, resolving errors of almost 40% otherwise seen for the case of dense bone phantoms at 80 kVp. Results are also presented for patient studies involving multiple CT scans at different kVp settings, which should all lead to the same 511 keV linear attenuation values. A linear fit to values obtained from 140 kVp CT images using the kVp-dependent scaling plotted as a function of the corresponding values obtained from 80 kVp CT images yielded y = 1.003 x -0.001 with an R2 value of 0.999, indicating that the same values are obtained to a high degree of accuracy.
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            Selectivity for conspecific song in the zebra finch auditory forebrain.

            The selectivity of neurons in the zebra finch auditory forebrain for natural sounds was investigated systematically. The principal auditory forebrain area in songbirds consists of the tonotopically organized field L complex, which, by its location in the auditory processing stream, can be compared with the auditory cortex of mammals. We also recorded from a secondary auditory area, cHV. Field L and cHV are auditory processing stages that are presynaptic to the specialized song system nuclei where auditory neurons show an extremely selective response for the bird's own song, but weak response to almost any other sounds, including conspecific songs. In our study, we found that neurons in field L and cHV had stronger responses to conspecific song than to synthetic sounds that were designed to match the lower order acoustical properties of song, such as their overall power spectra and AM spectra. Such preferential responses to natural sounds cannot be explained by linear frequency tuning or simple nonlinear intensity tuning and requires linear or nonlinear spectro-temporal neuronal transfer functions tuned to the acoustical properties of song. The selectivity for conspecific songs in field L and cHV might reflect an intermediate auditory processing stage for vocalizations that then contributes to the generation of the very specific selectivity for the bird's own song seen in the postsynaptic song system.
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              Spatial resolution and sensitivity of the Inveon small-animal PET scanner.

              The Inveon small-animal PET scanner is characterized by a large, 127-mm axial length and a 161-mm crystal ring diameter. The associated high sensitivity is obtained by using all lines of response (LORs) up to the maximum ring difference (MRD) of 79, for which the most oblique LORs form acceptance angles of 38.3 degrees with transaxial planes. The result is 2 phenomena that are normally not encountered in PET scanners: a parallax or depth-of-interaction effect in the axial direction and the breakdown of Fourier rebinning (FORE). Both effects cause a deterioration of axial spatial resolution. Limiting the MRD to smaller values reduces this axial blurring at the cost of sensitivity. Alternatively, 3-dimensional (3D) reconstruction techniques can be used in which the rebinning step is absent. The aim of this study was to experimentally determine the spatial resolution and sensitivity of the Inveon for its whole field of view (FOV). Spatial resolution and sensitivity were measured using filtered backprojection (FBP) with FORE, FBP with LOR angle-weighted adapted FORE (AFORE), and 3D ordered-subset expectation maximization followed by maximum a posteriori reconstruction (OSEM3D/MAP). Tangential and radial full width at half maximum (FWHM) showed almost no dependence on the MRD using FORE and FBP. Tangential FWHMs were 1.5 mm in the center of the FOV (CFOV) and 1.8 mm at the edge of the FOV (EFOV). Radial FWHMs were 1.5 and 3.0 mm in the CFOV and EFOV, respectively. In contrast, axial FWHMs increased with the MRD and ranged between 1.1 and 2.0 mm in the CFOV and between 1.5 and 2.7 mm in the EFOV for a MRD between 1 and 79. AFORE improved the axial resolution for a large part of the FOV, but image noise increased. OSEM3D/MAP yielded uniform spatial resolution in all directions, with an average FWHM of 1.65+/-0.06 mm. Sensitivity in the CFOV for the default energy and coincidence time window was 0.068; peak sensitivity was 0.111. The Inveon showed high spatial resolution and high sensitivity, both of which can be maintained using OSEM3D/MAP reconstruction instead of rebinning and 2D algorithms.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 August 2017
                2017
                : 12
                : 8
                : e0182875
                Affiliations
                [1 ] Department of Radiology and Biomedical Imaging, Yale Positron Emission Tomography Center, Yale University, New Haven, Connecticut, United States of America
                [2 ] Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States of America
                Texas Christian University, UNITED STATES
                Author notes

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

                Author information
                http://orcid.org/0000-0003-4030-4212
                Article
                PONE-D-17-12102
                10.1371/journal.pone.0182875
                5568339
                28832614
                aa09edd8-164a-4876-a963-e99a416fdd06
                © 2017 Lattin et al

                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
                : 28 March 2017
                : 26 July 2017
                Page count
                Figures: 4, Tables: 1, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100009559, Life Sciences Research Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006405, American Ornithologists' Union;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100001461, American Philosophical Society;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 1S10OD010322-01
                Award Recipient :
                This study was funded by the Howard Hughes Medical Institute Fellowship of the Life Sciences Research Foundation ( http://www.lsrf.org/); American Ornithologists' Union ( http://www.americanornithology.org/); American Philosophical Society ( https://www.amphilsoc.org/) to CRL; and the National Institutes of Health grant 1S10OD010322-01 ( https://www.nih.gov/) to REC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Estradiol
                Research and Analysis Methods
                Imaging Techniques
                Neuroimaging
                Positron Emission Tomography
                Biology and Life Sciences
                Neuroscience
                Neuroimaging
                Positron Emission Tomography
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Tomography
                Positron Emission Tomography
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Tomography
                Positron Emission Tomography
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Tomography
                Positron Emission Tomography
                Biology and Life Sciences
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                Amniotes
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                Neuroimaging
                Biology and Life Sciences
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                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Signaling and Communication
                Bird Song
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Signaling and Communication
                Bird Song
                Biology and Life Sciences
                Zoology
                Ornithology
                Bird Song
                Biology and Life Sciences
                Organisms
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                Birds
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                Research and Analysis Methods
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                Neuroimaging
                Computed Axial Tomography
                Biology and Life Sciences
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                Medicine and Health Sciences
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                Diagnostic Radiology
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                Computed Axial Tomography
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                Imaging Techniques
                Diagnostic Radiology
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                Computed Axial Tomography
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Tomography
                Computed Axial Tomography
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