Prenatal lead exposure impacts cross-hemispheric and long-range connectivity in the human fetal brain
Lead represents a highly prevalent metal toxicant with potential to alter human biology in lasting ways. A population segment that is particularly vulnerable to the negative consequences of lead exposure is the human fetus, as exposure events occurring before birth are linked to varied and long-rang...
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Published in | NeuroImage (Orlando, Fla.) Vol. 191; pp. 186 - 192 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
01.05.2019
Elsevier Limited |
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Abstract | Lead represents a highly prevalent metal toxicant with potential to alter human biology in lasting ways. A population segment that is particularly vulnerable to the negative consequences of lead exposure is the human fetus, as exposure events occurring before birth are linked to varied and long-ranging negative health and behavioral outcomes. An area that has yet to be addressed is the potential that lead exposure during pregnancy alters brain development even before an individual is born. Here, we combine prenatal lead exposure information extracted from newborn bloodspots with the human fetal brain functional MRI data to assess whether neural network connectivity differs between lead-exposed and lead-naïve fetuses. We found that neural connectivity patterns differed in lead-exposed and comparison groups such that fetuses that were not exposed demonstrated stronger age-related increases in cross-hemispheric connectivity, while the lead-exposed group demonstrated stronger age-related increases in posterior cingulate cortex (PCC) to lateral prefrontal cortex (PFC) connectivity. These are the first results to demonstrate metal toxicant-related alterations in human fetal neural connectivity. Remarkably, the findings point to alterations in systems that support higher-order cognitive and regulatory functions. Objectives for future work are to replicate these results in larger samples and to test the possibility that these alterations may account for significant variation in future child cognitive and behavioral outcomes.
•In humans, prenatal exposure to lead relates to connectivity of large-scale fetal brain systems.•Age-related strengthening of insular/temporal cross-hemispheric functional connectivity was stronger in fetuses that did not appear to have been exposed to lead.•Fetuses exposed to lead showed age-related strengthening of lateral prefrontal to posterior cingulate functional connectivity. |
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AbstractList | Lead represents a highly prevalent metal toxicant with potential to alter human biology in lasting ways. A population segment that is particularly vulnerable to the negative consequences of lead exposure is the human fetus, as exposure events occurring before birth are linked to varied and long-ranging negative health and behavioral outcomes. An area that has yet to be addressed is the potential that lead exposure during pregnancy alters brain development even before an individual is born. Here, we combine prenatal lead exposure information extracted from newborn bloodspots with the human fetal brain functional MRI data to assess whether neural network connectivity differs between lead-exposed and lead-naïve fetuses. We found that neural connectivity patterns differed in lead-exposed and comparison groups such that fetuses that were not exposed demonstrated stronger age-related increases in cross-hemispheric connectivity, while the lead-exposed group demonstrated stronger age-related increases in posterior cingulate cortex (PCC) to lateral prefrontal cortex (PFC) connectivity. These are the first results to demonstrate metal toxicant-related alterations in human fetal neural connectivity. Remarkably, the findings point to alterations in systems that support higher-order cognitive and regulatory functions. Objectives for future work are to replicate these results in larger samples and to test the possibility that these alterations may account for significant variation in future child cognitive and behavioral outcomes.
•In humans, prenatal exposure to lead relates to connectivity of large-scale fetal brain systems.•Age-related strengthening of insular/temporal cross-hemispheric functional connectivity was stronger in fetuses that did not appear to have been exposed to lead.•Fetuses exposed to lead showed age-related strengthening of lateral prefrontal to posterior cingulate functional connectivity. Lead represents a highly prevalent metal toxicant with potential to alter human biology in lasting ways. A population segment that is particularly vulnerable to the negative consequences of lead exposure is the human fetus, as exposure events occurring before birth are linked to varied and long-ranging negative health and behavioral outcomes. An area that has yet to be addressed is the potential that lead exposure during pregnancy alters brain development even before an individual is born. Here, we combine prenatal lead exposure information extracted from newborn bloodspots with the human fetal brain functional MRI data to assess whether neural network connectivity differs between lead-exposed and lead-naïve fetuses. We found that neural connectivity patterns differed in lead-exposed and comparison groups such that fetuses that were not exposed demonstrated stronger age-related increases in cross-hemispheric connectivity, while the lead-exposed group demonstrated stronger age-related increases in posterior cingulate cortex (PCC) to lateral prefrontal cortex (PFC) connectivity. These are the first results to demonstrate metal toxicant-related alterations in human fetal neural connectivity. Remarkably, the findings point to alterations in systems that support higher-order cognitive and regulatory functions. Objectives for future work are to replicate these results in larger samples and to test the possibility that these alterations may account for significant variation in future child cognitive and behavioral outcomes. |
Author | Rauh, Virginia A. Thomason, Moriah E. Trentacosta, Christopher Eggebrecht, Adam T. Espinoza-Heredia, Claudia Wheelock, Muriah D. Burt, S. Alexandra Hect, Jasmine L. |
AuthorAffiliation | 2 Department of Population Health, New York University Medical Center, New York, NY, USA 3 Institute for Social Research, University of Michigan, Ann Arbor, MI, USA 6 Department of Psychiatry, Washington University in St. Louis, St. Louis, MO, USA 1 Department of Child and Adolescent Psychiatry, New York University Medical Center, New York, USA 8 Department of Psychology, Michigan State University, East Lansing, MI, USA 5 The Heilbrunn Department of Population & Family Health, Columbia University Medical Center, New York, NY, USA 7 Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO, USA 4 Department of Psychology, Wayne State University, Detroit, MI, USA |
AuthorAffiliation_xml | – name: 1 Department of Child and Adolescent Psychiatry, New York University Medical Center, New York, USA – name: 6 Department of Psychiatry, Washington University in St. Louis, St. Louis, MO, USA – name: 2 Department of Population Health, New York University Medical Center, New York, NY, USA – name: 8 Department of Psychology, Michigan State University, East Lansing, MI, USA – name: 5 The Heilbrunn Department of Population & Family Health, Columbia University Medical Center, New York, NY, USA – name: 4 Department of Psychology, Wayne State University, Detroit, MI, USA – name: 3 Institute for Social Research, University of Michigan, Ann Arbor, MI, USA – name: 7 Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO, USA |
Author_xml | – sequence: 1 givenname: Moriah E. surname: Thomason fullname: Thomason, Moriah E. email: moriah.thomason@nyulangone.org organization: Department of Child and Adolescent Psychiatry, New York University Medical Center, New York, USA – sequence: 2 givenname: Jasmine L. surname: Hect fullname: Hect, Jasmine L. organization: Department of Psychology, Wayne State University, Detroit, MI, USA – sequence: 3 givenname: Virginia A. surname: Rauh fullname: Rauh, Virginia A. organization: The Heilbrunn Department of Population & Family Health, Columbia University Medical Center, New York, NY, USA – sequence: 4 givenname: Christopher surname: Trentacosta fullname: Trentacosta, Christopher organization: Department of Psychology, Wayne State University, Detroit, MI, USA – sequence: 5 givenname: Muriah D. surname: Wheelock fullname: Wheelock, Muriah D. organization: Department of Psychiatry, Washington University in St. Louis, St. Louis, MO, USA – sequence: 6 givenname: Adam T. surname: Eggebrecht fullname: Eggebrecht, Adam T. organization: Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO, USA – sequence: 7 givenname: Claudia surname: Espinoza-Heredia fullname: Espinoza-Heredia, Claudia organization: Department of Child and Adolescent Psychiatry, New York University Medical Center, New York, USA – sequence: 8 givenname: S. Alexandra surname: Burt fullname: Burt, S. Alexandra organization: Department of Psychology, Michigan State University, East Lansing, MI, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30739062$$D View this record in MEDLINE/PubMed |
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Keywords | Prenatal Brain MRI Lead Connectivity Resting-state Fetal |
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SubjectTerms | Age Animal cognition Brain Brain - drug effects Brain - pathology Cognitive ability Connectivity Consent Cortex (cingulate) Female Fetal Fetus Fetuses Functional magnetic resonance imaging Humans Lead Lead - adverse effects Lead poisoning Lead Poisoning, Nervous System, Childhood - pathology Magnetic Resonance Imaging - methods Medical screening Mothers MRI Nervous system Neural networks Neural Pathways - drug effects Neural Pathways - pathology NMR Nuclear magnetic resonance Prefrontal cortex Pregnancy Prenatal Prenatal Diagnosis Prenatal experience Prenatal Exposure Delayed Effects - etiology Prenatal Exposure Delayed Effects - pathology Resting-state |
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Title | Prenatal lead exposure impacts cross-hemispheric and long-range connectivity in the human fetal brain |
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