Altered Hippocampal-Prefrontal Neural Dynamics in Mouse Models of Down Syndrome

Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC el...

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Published inCell reports (Cambridge) Vol. 30; no. 4; pp. 1152 - 1163.e4
Main Authors Chang, Pishan, Bush, Daniel, Schorge, Stephanie, Good, Mark, Canonica, Tara, Shing, Nathanael, Noy, Suzanna, Wiseman, Frances K., Burgess, Neil, Tybulewicz, Victor L.J., Walker, Matthew C., Fisher, Elizabeth M.C.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 28.01.2020
Cell Press
Elsevier
Subjects
Animals
Chromosomes, Human, Pair 21 - genetics
Cognitive Dysfunction - genetics
Cognitive Dysfunction - physiopathology
Disease Models, Animal
Down syndrome
Down Syndrome - genetics
Dyrk Kinases
Electroencephalography
executive function
functional connectivity
gamma
hippocampus
Hippocampus - metabolism
Hippocampus - physiopathology
Humans
Male
memory
Memory, Short-Term - physiology
Mice
Mice, Inbred C57BL
prefrontal cortex
Prefrontal Cortex - metabolism
Prefrontal Cortex - physiology
Protein Serine-Threonine Kinases - genetics
Protein Serine-Threonine Kinases - metabolism
Protein-Tyrosine Kinases - genetics
Protein-Tyrosine Kinases - metabolism
Spatial Memory - physiology
theta
Theta Rhythm - genetics
Trisomy - genetics
Trisomy - physiopathology
Trisomy 21
Trisomy 21
memory
functional connectivity
hippocampus
prefrontal cortex
Down syndrome
theta
gamma
executive function
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Abstract Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21. [Display omitted] •Study of behavior and EEG in three partially trisomic mouse models of Down syndrome (DS)•These mutant mice show non-overlapping differences in spatial working memory function•Behavioral changes segregate with distinct EEG abnormalities in the hippocampus and mPFC•This links cognitive deficits to specific changes in hippocampal and mPFC circuit dynamics Chang et al. examine three partially trisomic mouse models of Down syndrome that together cover all regions of homology with human chromosome 21. They identify non-overlapping differences in spatial working memory function associated with distinct abnormalities in hippocampal and medial prefrontal electrophysiology.
AbstractList Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21.Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21.
Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21. [Display omitted] •Study of behavior and EEG in three partially trisomic mouse models of Down syndrome (DS)•These mutant mice show non-overlapping differences in spatial working memory function•Behavioral changes segregate with distinct EEG abnormalities in the hippocampus and mPFC•This links cognitive deficits to specific changes in hippocampal and mPFC circuit dynamics Chang et al. examine three partially trisomic mouse models of Down syndrome that together cover all regions of homology with human chromosome 21. They identify non-overlapping differences in spatial working memory function associated with distinct abnormalities in hippocampal and medial prefrontal electrophysiology.
Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A , which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21. • Study of behavior and EEG in three partially trisomic mouse models of Down syndrome (DS) • These mutant mice show non-overlapping differences in spatial working memory function • Behavioral changes segregate with distinct EEG abnormalities in the hippocampus and mPFC • This links cognitive deficits to specific changes in hippocampal and mPFC circuit dynamics Chang et al. examine three partially trisomic mouse models of Down syndrome that together cover all regions of homology with human chromosome 21. They identify non-overlapping differences in spatial working memory function associated with distinct abnormalities in hippocampal and medial prefrontal electrophysiology.
Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21. : Chang et al. examine three partially trisomic mouse models of Down syndrome that together cover all regions of homology with human chromosome 21. They identify non-overlapping differences in spatial working memory function associated with distinct abnormalities in hippocampal and medial prefrontal electrophysiology. Keywords: Down syndrome, Trisomy 21, hippocampus, prefrontal cortex, memory, executive function, theta, gamma, functional connectivity
Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down syndrome (DS). Here, we demonstrate non-overlapping behavioral differences associated with distinct abnormalities in hippocampal and mPFC electrophysiology during a canonical spatial working memory task in three partially trisomic mouse models of DS (Dp1Tyb, Dp10Yey, and Dp17Yey) that together cover all regions of homology with human chromosome 21 (Hsa21). Dp1Tyb mice show slower decision-making (unrelated to the gene dose of DYRK1A, which has been implicated in DS cognitive dysfunction) and altered theta dynamics (reduced frequency, increased hippocampal-mPFC coherence, and increased modulation of hippocampal high gamma); Dp10Yey mice show impaired alternation performance and reduced theta modulation of hippocampal low gamma; and Dp17Yey mice are not significantly different from the wild type. These results link specific hippocampal and mPFC circuit dysfunctions to cognitive deficits in DS models and, importantly, map them to discrete regions of Hsa21.
Author Tybulewicz, Victor L.J.
Fisher, Elizabeth M.C.
Chang, Pishan
Good, Mark
Noy, Suzanna
Burgess, Neil
Bush, Daniel
Canonica, Tara
Shing, Nathanael
Walker, Matthew C.
Schorge, Stephanie
Wiseman, Frances K.
AuthorAffiliation 3 UCL Institute of Cognitive Neuroscience, UCL Queen Square Institute of Neurology, University College London WC1N 3AZ, UK
6 Department of Medicine, Imperial College, London W12 0NN, UK
2 Department of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London WC1N 3BG, UK
4 School of Psychology, College of Biomedical and Life Sciences, Cardiff University, Cardiff CF10 3AT, UK
5 Francis Crick Institute, London NW1 1AT, UK
1 Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London WC1N 3BG, UK
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Issue 4
Keywords Trisomy 21
memory
functional connectivity
hippocampus
prefrontal cortex
Down syndrome
theta
gamma
executive function
Language English
License This is an open access article under the CC BY license.
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Snippet Altered neural dynamics in the medial prefrontal cortex (mPFC) and hippocampus may contribute to cognitive impairments in the complex chromosomal disorder Down...
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StartPage 1152
SubjectTerms Animals
Chromosomes, Human, Pair 21 - genetics
Cognitive Dysfunction - genetics
Cognitive Dysfunction - physiopathology
Disease Models, Animal
Down syndrome
Down Syndrome - genetics
Dyrk Kinases
Electroencephalography
executive function
functional connectivity
gamma
hippocampus
Hippocampus - metabolism
Hippocampus - physiopathology
Humans
Male
memory
Memory, Short-Term - physiology
Mice
Mice, Inbred C57BL
prefrontal cortex
Prefrontal Cortex - metabolism
Prefrontal Cortex - physiology
Protein Serine-Threonine Kinases - genetics
Protein Serine-Threonine Kinases - metabolism
Protein-Tyrosine Kinases - genetics
Protein-Tyrosine Kinases - metabolism
Spatial Memory - physiology
theta
Theta Rhythm - genetics
Trisomy - genetics
Trisomy - physiopathology
Trisomy 21
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Title Altered Hippocampal-Prefrontal Neural Dynamics in Mouse Models of Down Syndrome
URI https://dx.doi.org/10.1016/j.celrep.2019.12.065
https://www.ncbi.nlm.nih.gov/pubmed/31995755
https://www.proquest.com/docview/2348800670
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https://doaj.org/article/0726a09e79f942f28afb7ca0608d677c
Volume 30
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