Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver

Neuron. 2013 Apr 10;78(1):81-93. doi: 10.1016/j.neuron.2013.02.011.

Abstract

The hippocampus in schizophrenia is characterized by both hypermetabolism and reduced size. It remains unknown whether these abnormalities are mechanistically linked. Here we addressed this question by using MRI tools that can map hippocampal metabolism and structure in patients and mouse models. In at-risk patients, hypermetabolism was found to begin in CA1 and spread to the subiculum after psychosis onset. CA1 hypermetabolism at baseline predicted hippocampal atrophy, which occurred during progression to psychosis, most prominently in similar regions. Next, we used ketamine to model conditions of acute psychosis in mice. Acute ketamine reproduced a similar regional pattern of hypermetabolism, while repeated exposure shifted the hippocampus to a hypermetabolic basal state with concurrent atrophy and pathology in parvalbumin-expressing interneurons. Parallel in vivo experiments using the glutamate-reducing drug LY379268 and direct measurements of extracellular glutamate showed that glutamate drives both neuroimaging abnormalities. These findings show that hippocampal hypermetabolism leads to atrophy in psychotic disorder and suggest glutamate as a pathogenic driver.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Amino Acids / pharmacology
  • Animals
  • Atrophy / chemically induced
  • Brain Mapping*
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Disease Models, Animal
  • Excitatory Amino Acid Agonists / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • Follow-Up Studies
  • Functional Laterality / drug effects
  • Glutamic Acid / metabolism*
  • Hippocampus / blood supply
  • Hippocampus / drug effects
  • Hippocampus / pathology*
  • Humans
  • Imaging, Three-Dimensional
  • Ketamine / toxicity
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Psychotic Disorders / etiology
  • Psychotic Disorders / pathology*
  • Time Factors

Substances

  • Amino Acids
  • Bridged Bicyclo Compounds, Heterocyclic
  • Excitatory Amino Acid Agonists
  • Excitatory Amino Acid Antagonists
  • LY 379268
  • Glutamic Acid
  • Ketamine