Neural synchronization deficits linked to cortical hyper-excitability and auditory hypersensitivity in fragile X syndrome

Mol Autism. 2017 Jun 7:8:22. doi: 10.1186/s13229-017-0140-1. eCollection 2017.

Abstract

Background: Studies in the fmr1 KO mouse demonstrate hyper-excitability and increased high-frequency neuronal activity in sensory cortex. These abnormalities may contribute to prominent and distressing sensory hypersensitivities in patients with fragile X syndrome (FXS). The current study investigated functional properties of auditory cortex using a sensory entrainment task in FXS.

Methods: EEG recordings were obtained from 17 adolescents and adults with FXS and 17 age- and sex-matched healthy controls. Participants heard an auditory chirp stimulus generated using a 1000-Hz tone that was amplitude modulated by a sinusoid linearly increasing in frequency from 0-100 Hz over 2 s.

Results: Single trial time-frequency analyses revealed decreased gamma band phase-locking to the chirp stimulus in FXS, which was strongly coupled with broadband increases in gamma power. Abnormalities in gamma phase-locking and power were also associated with theta-gamma amplitude-amplitude coupling during the pre-stimulus period and with parent reports of heightened sensory sensitivities and social communication deficits.

Conclusions: This represents the first demonstration of neural entrainment alterations in FXS patients and suggests that fast-spiking interneurons regulating synchronous high-frequency neural activity have reduced functionality. This reduced ability to synchronize high-frequency neural activity was related to the total power of background gamma band activity. These observations extend findings from fmr1 KO models of FXS, characterize a core pathophysiological aspect of FXS, and may provide a translational biomarker strategy for evaluating promising therapeutics.

Keywords: Chirp; EEG; Fragile X syndrome; Gamma; Sensory.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acoustic Stimulation
  • Adolescent
  • Adult
  • Auditory Cortex / metabolism
  • Auditory Cortex / physiopathology*
  • Case-Control Studies
  • Electroencephalography
  • Evoked Potentials, Auditory*
  • Female
  • Fragile X Mental Retardation Protein / genetics*
  • Fragile X Syndrome / diagnosis
  • Fragile X Syndrome / genetics
  • Fragile X Syndrome / physiopathology*
  • Gene Expression
  • Humans
  • Hyperkinesis / diagnosis
  • Hyperkinesis / genetics
  • Hyperkinesis / physiopathology*
  • Interneurons / metabolism
  • Interneurons / pathology
  • Male
  • Middle Aged
  • Mutation
  • Social Communication Disorder / diagnosis
  • Social Communication Disorder / genetics
  • Social Communication Disorder / physiopathology*

Substances

  • FMR1 protein, human
  • Fragile X Mental Retardation Protein