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Keywords:

  • carbachol;
  • kainate;
  • phase coupling;
  • synchronization;
  • theta rhythm

Abstract

Synchronization of neuronal activity in the visual cortex at low (30–70 Hz) and high gamma band frequencies (> 70 Hz) has been associated with distinct visual processes, but mechanisms underlying high-frequency gamma oscillations remain unknown. In rat visual cortex slices, kainate and carbachol induce high-frequency gamma oscillations (fast-γ; peak frequency ∼ 80 Hz at 37°C) that can coexist with low-frequency gamma oscillations (slow-γ; peak frequency ∼ 50 Hz at 37°C) in the same column. Current-source density analysis showed that fast-γ was associated with rhythmic current sink-source sequences in layer III and slow-γ with rhythmic current sink-source sequences in layer V. Fast-γ and slow-γ were not phase-locked. Slow-γ power fluctuations were unrelated to fast-γ power fluctuations, but were modulated by the phase of theta (3–8 Hz) oscillations generated in the deep layers. Fast-γ was spatially less coherent than slow-γ. Fast-γ and slow-γ were dependent on γ-aminobutyric acid (GABA)A receptors, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors and gap-junctions, their frequencies were reduced by thiopental and were weakly dependent on cycle amplitude. Fast-γ and slow-γ power were differentially modulated by thiopental and adenosine A1 receptor blockade, and their frequencies were differentially modulated by N-methyl-d-aspartate (NMDA) receptors, GluK1 subunit-containing receptors and persistent sodium currents. Our data indicate that fast-γ and slow-γ both depend on and are paced by recurrent inhibition, but have distinct pharmacological modulation profiles. The independent co-existence of fast-γ and slow-γ allows parallel processing of distinct aspects of vision and visual perception. The visual cortex slice provides a novel in vitro model to study cortical high-frequency gamma oscillations.