COMT and DRD2/ANKK-1 gene-gene interaction account for resetting of gamma neural oscillations to auditory stimulus-driven attention

PLoS One. 2017 Feb 21;12(2):e0172362. doi: 10.1371/journal.pone.0172362. eCollection 2017.

Abstract

Attention capture by potentially relevant environmental stimuli is critical for human survival, yet it varies considerably among individuals. A large series of studies has suggested that attention capture may depend on the cognitive balance between maintenance and manipulation of mental representations and the flexible switch between goal-directed representations and potentially relevant stimuli outside the focus of attention; a balance that seems modulated by a prefrontostriatal dopamine pathway. Here, we examined inter-individual differences in the cognitive control of attention through studying the effects of two single nucleotide polymorphisms regulating dopamine at the prefrontal cortex and the striatum (i.e., COMTMet108/158Val and ANKK1/DRD2TaqIA) on stimulus-driven attention capture. Healthy adult participants (N = 40) were assigned to different groups according to the combination of the polymorphisms COMTMet108/158Val and ANKK1/DRD2TaqIA, and were instructed to perform on a well-established distraction protocol. Performance in individuals with a balance between prefrontal dopamine display and striatal receptor density was slowed down by the occurrence of unexpected distracting events, while those with a rather unbalanced dopamine activity were able maintain task performance with no time delay, yet at the expense of a slightly lower accuracy. This advantage, associated to their distinct genetic profiles, was paralleled by an electrophysiological mechanism of phase-resetting of gamma neural oscillation to the novel, distracting events. Taken together, the current results suggest that the epistatic interaction between COMTVal108/158Met and ANKK1/DRD2 TaqIa genetic polymorphisms lies at the basis of stimulus-driven attention capture.

MeSH terms

  • Acoustic Stimulation*
  • Adolescent
  • Adult
  • Attention / physiology*
  • Catechol O-Methyltransferase / genetics*
  • Catechol O-Methyltransferase / physiology
  • Corpus Striatum / physiology
  • Epistasis, Genetic*
  • Female
  • Gamma Rhythm / physiology*
  • Humans
  • Male
  • Memory, Short-Term / physiology
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / physiology
  • Neuropsychological Tests
  • Polymorphism, Single Nucleotide*
  • Prefrontal Cortex / physiology
  • Protein Serine-Threonine Kinases / genetics*
  • Protein Serine-Threonine Kinases / physiology
  • Receptors, Dopamine D2 / genetics*
  • Receptors, Dopamine D2 / physiology
  • Time Factors
  • Young Adult

Substances

  • DRD2 protein, human
  • Nerve Tissue Proteins
  • Receptors, Dopamine D2
  • COMT protein, human
  • Catechol O-Methyltransferase
  • ANKK1 protein, human
  • Protein Serine-Threonine Kinases

Grants and funding

This work was supported by grants from the Spanish Ministry of Economy and Knowledge(PSI 2015-63664-P), the Catalan Government (SGR2014-177), and the ICREA Academia Distinguished Professorship awarded to CE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.