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      Human amygdala functional network development: A cross-sectional study from 3 months to 5 years of age

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          Abstract

          Although the amygdala’s role in shaping social behavior is especially important during early post-natal development, very little is known of amygdala functional development before childhood. To address this gap, this study uses resting-state fMRI to examine early amygdalar functional network development in a cross-sectional sample of 80 children from 3-months to 5-years of age. Whole brain functional connectivity with the amygdala, and its laterobasal and superficial sub-regions, were largely similar to those seen in older children and adults. Functional distinctions between sub-region networks were already established. These patterns suggest many amygdala functional circuits are intact from infancy, especially those that are part of motor, visual, auditory and subcortical networks. Developmental changes in connectivity were observed between the laterobasal nucleus and bilateral ventral temporal and motor cortex as well as between the superficial nuclei and medial thalamus, occipital cortex and a different region of motor cortex. These results show amygdala-subcortical and sensory-cortex connectivity begins refinement prior to childhood, though connectivity changes with associative and frontal cortical areas, seen after early childhood, were not evident in this age range. These findings represent early steps in understanding amygdala network dynamics across infancy through early childhood, an important period of emotional and cognitive development.

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          Most cited references 101

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          Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization.

          Resting state functional connectivity MRI (fcMRI) is widely used to investigate brain networks that exhibit correlated fluctuations. While fcMRI does not provide direct measurement of anatomic connectivity, accumulating evidence suggests it is sufficiently constrained by anatomy to allow the architecture of distinct brain systems to be characterized. fcMRI is particularly useful for characterizing large-scale systems that span distributed areas (e.g., polysynaptic cortical pathways, cerebro-cerebellar circuits, cortical-thalamic circuits) and has complementary strengths when contrasted with the other major tool available for human connectomics-high angular resolution diffusion imaging (HARDI). We review what is known about fcMRI and then explore fcMRI data reliability, effects of preprocessing, analysis procedures, and effects of different acquisition parameters across six studies (n = 98) to provide recommendations for optimization. Run length (2-12 min), run structure (1 12-min run or 2 6-min runs), temporal resolution (2.5 or 5.0 s), spatial resolution (2 or 3 mm), and the task (fixation, eyes closed rest, eyes open rest, continuous word-classification) were varied. Results revealed moderate to high test-retest reliability. Run structure, temporal resolution, and spatial resolution minimally influenced fcMRI results while fixation and eyes open rest yielded stronger correlations as contrasted to other task conditions. Commonly used preprocessing steps involving regression of nuisance signals minimized nonspecific (noise) correlations including those associated with respiration. The most surprising finding was that estimates of correlation strengths stabilized with acquisition times as brief as 5 min. The brevity and robustness of fcMRI positions it as a powerful tool for large-scale explorations of genetic influences on brain architecture. We conclude by discussing the strengths and limitations of fcMRI and how it can be combined with HARDI techniques to support the emerging field of human connectomics.
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            Neurobiology of emotion perception I: The neural basis of normal emotion perception.

            There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.
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              Socioeconomic status and the developing brain.

              Childhood socioeconomic status (SES) is associated with cognitive achievement throughout life. How does SES relate to brain development, and what are the mechanisms by which SES might exert its influence? We review studies in which behavioral, electrophysiological and neuroimaging methods have been used to characterize SES disparities in neurocognitive function. These studies indicate that SES is an important predictor of neurocognitive performance, particularly of language and executive function, and that SES differences are found in neural processing even when performance levels are equal. Implications for basic cognitive neuroscience and for understanding and ameliorating the problems related to childhood poverty are discussed.
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                Author and article information

                Contributors
                Journal
                Dev Cogn Neurosci
                Dev Cogn Neurosci
                Developmental Cognitive Neuroscience
                Elsevier
                1878-9293
                1878-9307
                1 November 2018
                November 2018
                : 34
                : 63-74
                Affiliations
                [a ]Division of Developmental Medicine, Boston Children’s Hospital, Harvard University, Boston, MA, 02115, USA
                [b ]Department of Forensic and Neurodevelopmental Sciences & Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK
                [c ]Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering & Imaging Sciences, King’s College London, London, UK
                [d ]Advanced Baby Imaging Lab, Brown University School of Engineering, Providence, USA
                [e ]Waisman Center, University of Wisconsin-Madison, Madison, WI, 53702, USA
                [f ]Center for Healthy Minds, University of Wisconsin-Madison, Madison, WI, 53702, USA
                [g ]Department of Psychology, Columbia University, New York, NY, 10027, USA
                [h ]Department of Pediatrics, Warren Alpert Medical School, Brown University, Providence, USA
                Author notes
                [* ]Corresponing author at: Department of Forensic and Neurodevelopmental Sciences, Box PO50, De Crespigny Park, King’s College London, London, England, SE5 8AF, UK. jonathonom@ 123456kcl.ac.uk
                [1]

                Denotes equal contribution.

                Article
                S1878-9293(18)30046-X
                10.1016/j.dcn.2018.06.004
                6252269
                30075348
                © 2018 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                Categories
                Article

                Neurosciences

                amygdala, development, early childhood, resting-state, functional connectivity, infancy

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