Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task

The frontal cortex undergoes substantial structural and functional changes during adolescence and significant developmental changes also occur in the hippocampus. Both of these regions are notably vulnerable to alcohol and other substance use, which is typically initiated during adolescence. Identif...

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Main Authors: Jennifer T. Sneider, Julia E. Cohen-Gilbert, Derek A. Hamilton, Elena R. Stein, Noa Golan, Emily N. Oot, Anna M. Seraikas, Michael L. Rohan, Sion K. Harris, Lisa D. Nickerson, Marisa M. Silveri
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-06-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2018.00238/full
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author Jennifer T. Sneider
Jennifer T. Sneider
Julia E. Cohen-Gilbert
Julia E. Cohen-Gilbert
Derek A. Hamilton
Elena R. Stein
Noa Golan
Emily N. Oot
Emily N. Oot
Anna M. Seraikas
Michael L. Rohan
Michael L. Rohan
Sion K. Harris
Lisa D. Nickerson
Lisa D. Nickerson
Marisa M. Silveri
Marisa M. Silveri
Marisa M. Silveri
spellingShingle Jennifer T. Sneider
Jennifer T. Sneider
Julia E. Cohen-Gilbert
Julia E. Cohen-Gilbert
Derek A. Hamilton
Elena R. Stein
Noa Golan
Emily N. Oot
Emily N. Oot
Anna M. Seraikas
Michael L. Rohan
Michael L. Rohan
Sion K. Harris
Lisa D. Nickerson
Lisa D. Nickerson
Marisa M. Silveri
Marisa M. Silveri
Marisa M. Silveri
Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
Frontiers in Human Neuroscience
adolescence
BOLD fMRI
Morris water task
spatial memory
hippocampus
prefrontal cortex
author_facet Jennifer T. Sneider
Jennifer T. Sneider
Julia E. Cohen-Gilbert
Julia E. Cohen-Gilbert
Derek A. Hamilton
Elena R. Stein
Noa Golan
Emily N. Oot
Emily N. Oot
Anna M. Seraikas
Michael L. Rohan
Michael L. Rohan
Sion K. Harris
Lisa D. Nickerson
Lisa D. Nickerson
Marisa M. Silveri
Marisa M. Silveri
Marisa M. Silveri
author_sort Jennifer T. Sneider
title Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
title_short Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
title_full Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
title_fullStr Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
title_full_unstemmed Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water Task
title_sort adolescent hippocampal and prefrontal brain activation during performance of the virtual morris water task
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2018-06-01
description The frontal cortex undergoes substantial structural and functional changes during adolescence and significant developmental changes also occur in the hippocampus. Both of these regions are notably vulnerable to alcohol and other substance use, which is typically initiated during adolescence. Identifying measures of brain function during adolescence, particularly before initiation of drug or alcohol use, is critical to understanding how such behaviors may affect brain development, especially in these vulnerable brain regions. While there is a substantial developmental literature on adolescent working memory, less is known about spatial memory. Thus, a virtual Morris water task (vMWT) was applied to probe function of the adolescent hippocampus. Multiband blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) data were acquired at 3T during task performance. Participants included 32 healthy, alcohol- and drug-naïve adolescents, 13–14 years old, examined at baseline of a 3-year longitudinal MRI study. Significantly greater BOLD activation was observed in the hippocampus and surrounding areas, and in prefrontal regions involved in executive function, during retrieval relative to motor performance. In contrast, significantly greater BOLD activation was observed in components of the default mode network, including frontal medial cortex, during the motor condition (when task demands were minimal) relative to the retrieval condition. Worse performance (longer path length) during retrieval was associated with greater activation of angular gyrus/supramarginal gyrus, whereas worse performance (longer path length/latency) during motor control was associated with less activation of frontal pole. Furthermore, while latency (time to complete task) was greater in females than in males, there were no sex differences in path length (accuracy), suggesting that females required more time to navigate the virtual environment, but did so as effectively as males. These findings demonstrate that performance of the vMWT elicits hippocampal and prefrontal activation patterns in early adolescence, similar to activation observed during spatial memory retrieval in adults. Given that this task is sensitive to hippocampal function, and that the adolescent hippocampus is notably vulnerable to the effects of alcohol and other substances, data acquired using this task during healthy adolescent development may provide a framework for understanding neurobiological impact of later initiation of use.
topic adolescence
BOLD fMRI
Morris water task
spatial memory
hippocampus
prefrontal cortex
url https://www.frontiersin.org/article/10.3389/fnhum.2018.00238/full
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spelling doaj-59aede5a92564d0c9437bc744b16a23f2020-11-25T03:00:56ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-06-011210.3389/fnhum.2018.00238375277Adolescent Hippocampal and Prefrontal Brain Activation During Performance of the Virtual Morris Water TaskJennifer T. Sneider0Jennifer T. Sneider1Julia E. Cohen-Gilbert2Julia E. Cohen-Gilbert3Derek A. Hamilton4Elena R. Stein5Noa Golan6Emily N. Oot7Emily N. Oot8Anna M. Seraikas9Michael L. Rohan10Michael L. Rohan11Sion K. Harris12Lisa D. Nickerson13Lisa D. Nickerson14Marisa M. Silveri15Marisa M. Silveri16Marisa M. Silveri17Neurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesDepartment of Psychiatry, Harvard Medical School, Harvard University, Boston, MA, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesDepartment of Psychiatry, Harvard Medical School, Harvard University, Boston, MA, United StatesDepartment of Psychology, University of New Mexico, Albuquerque, NM, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesSchool of Medicine, Boston University, Boston, MA, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesDepartment of Psychiatry, Harvard Medical School, Harvard University, Boston, MA, United StatesBrain Imaging Center, McLean Hospital, Belmont, MA, United StatesBoston Children’s Hospital, Harvard Medical School, Harvard University, Boston, MA, United StatesDepartment of Psychiatry, Harvard Medical School, Harvard University, Boston, MA, United StatesApplied Neuroimaging Statistics Laboratory, McLean Hospital, Belmont, MA, United StatesNeurodevelopmental Laboratory on Addictions and Mental Health, McLean Hospital, Belmont, MA, United StatesDepartment of Psychiatry, Harvard Medical School, Harvard University, Boston, MA, United StatesSchool of Medicine, Boston University, Boston, MA, United StatesThe frontal cortex undergoes substantial structural and functional changes during adolescence and significant developmental changes also occur in the hippocampus. Both of these regions are notably vulnerable to alcohol and other substance use, which is typically initiated during adolescence. Identifying measures of brain function during adolescence, particularly before initiation of drug or alcohol use, is critical to understanding how such behaviors may affect brain development, especially in these vulnerable brain regions. While there is a substantial developmental literature on adolescent working memory, less is known about spatial memory. Thus, a virtual Morris water task (vMWT) was applied to probe function of the adolescent hippocampus. Multiband blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) data were acquired at 3T during task performance. Participants included 32 healthy, alcohol- and drug-naïve adolescents, 13–14 years old, examined at baseline of a 3-year longitudinal MRI study. Significantly greater BOLD activation was observed in the hippocampus and surrounding areas, and in prefrontal regions involved in executive function, during retrieval relative to motor performance. In contrast, significantly greater BOLD activation was observed in components of the default mode network, including frontal medial cortex, during the motor condition (when task demands were minimal) relative to the retrieval condition. Worse performance (longer path length) during retrieval was associated with greater activation of angular gyrus/supramarginal gyrus, whereas worse performance (longer path length/latency) during motor control was associated with less activation of frontal pole. Furthermore, while latency (time to complete task) was greater in females than in males, there were no sex differences in path length (accuracy), suggesting that females required more time to navigate the virtual environment, but did so as effectively as males. These findings demonstrate that performance of the vMWT elicits hippocampal and prefrontal activation patterns in early adolescence, similar to activation observed during spatial memory retrieval in adults. Given that this task is sensitive to hippocampal function, and that the adolescent hippocampus is notably vulnerable to the effects of alcohol and other substances, data acquired using this task during healthy adolescent development may provide a framework for understanding neurobiological impact of later initiation of use.https://www.frontiersin.org/article/10.3389/fnhum.2018.00238/fulladolescenceBOLD fMRIMorris water taskspatial memoryhippocampusprefrontal cortex