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PMID: 27007844 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Thalamic reticular impairment underlies attention deficit in Ptchd1(Y/-) mice.

Nature ·Vol. 532 ·No. 7597 ·2016-04-07 ·Pages 58-63

Wells MF, Wimmer RD, Schmitt LI, Feng G, Halassa MM

Abstract

Developmental disabilities, including attention-deficit hyperactivity disorder (ADHD), intellectual disability (ID), and autism spectrum disorders (ASD), affect one in six children in the USA. Recently, gene mutations in patched domain containing 1 (PTCHD1) have been found in ~1% of patients with ID and ASD. Individuals with PTCHD1 deletion show symptoms of ADHD, sleep disruption, hypotonia, aggression, ASD, and ID. Although PTCHD1 is probably critical for normal development, the connection between its deletion and the ensuing behavioural defects is poorly understood. Here we report that during early post-natal development, mouse Ptchd1 is selectively expressed in the thalamic reticular nucleus (TRN), a group of GABAergic neurons that regulate thalamocortical transmission, sleep rhythms, and attention. Ptchd1 deletion attenuates TRN activity through mechanisms involving small conductance calcium-dependent potassium currents (SK). TRN-restricted deletion of Ptchd1 leads to attention deficits and hyperactivity, both of which are rescued by pharmacological augmentation of SK channel activity. Global Ptchd1 deletion recapitulates learning impairment, hyper-aggression, and motor defects, all of which are insensitive to SK pharmacological targeting and not found in the TRN-restricted deletion mouse. This study maps clinically relevant behavioural phenotypes onto TRN dysfunction in a human disease model, while also identifying molecular and circuit targets for intervention.

MeSH Terms
Aggression Animals Animals, Newborn Attention Attention Deficit Disorder with Hyperactivity/genetics,physiopathology,psychology Behavior, Animal Disease Models, Animal Electric Conductivity Female GABAergic Neurons/metabolism,pathology Gene Deletion Humans Learning Disabilities/genetics,physiopathology Male Membrane Proteins/deficiency,genetics,metabolism Mice Mice, Knockout Motor Disorders/genetics,physiopathology Neural Inhibition Potassium Channels, Calcium-Activated/metabolism Sleep Sleep Deprivation/genetics,physiopathology Thalamic Nuclei/pathology,physiopathology
Chemicals
Membrane Proteins Potassium Channels, Calcium-Activated Ptchd1 protein, mouse
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wells Michael F
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, USA. | McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
Wimmer Ralf D
Neuroscience Institute, New York University Langone Medical Center, New York, New York 10016, USA. | Department of Neuroscience and Physiology, New York University Langone Medical Center, New York, New York 10016, USA.
Schmitt L Ian
Neuroscience Institute, New York University Langone Medical Center, New York, New York 10016, USA. | Department of Neuroscience and Physiology, New York University Langone Medical Center, New York, New York 10016, USA.
Feng Guoping
McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA. | Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA.
Halassa Michael M
Neuroscience Institute, New York University Langone Medical Center, New York, New York 10016, USA. | Department of Neuroscience and Physiology, New York University Langone Medical Center, New York, New York 10016, USA. | Department of Psychiatry, New York University Langone Medical Center, New York, New York 10016, USA. | Center for Neural Science, New York University, New York, New York 1003, USA.
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2016-04-07
Epub
2016-00-23
Pages
58-63
Language
English
Region
England
NLM ID
0410462
PMCID
PMC4875756
Subset
IM
Grants
NIMH NIH HHS · R01MH097104 · United States
NIMH NIH HHS · R01 MH097104 · United States
NIMH NIH HHS · R01 MH107680 · United States
NIMH NIH HHS · R01MH10768 · United States
NINDS NIH HHS · R00 NS078115 · United States
NIMH NIH HHS · F31 MH098641 · United States
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