Modulation-specific and laminar-dependent effects of acetylcholine on visual responses in the rat primary visual cortex

PLoS One. 2013 Jul 2;8(7):e68430. doi: 10.1371/journal.pone.0068430. Print 2013.

Abstract

Acetylcholine (ACh) is secreted from cholinergic neurons in the basal forebrain to regions throughout the cerebral cortex, including the primary visual cortex (V1), and influences neuronal activities across all six layers via a form of diffuse extrasynaptic modulation termed volume transmission. To understand this effect in V1, we performed extracellular multi-point recordings of neuronal responses to drifting sinusoidal grating stimuli from the cortical layers of V1 in anesthetized rats and examined the modulatory effects of topically administered ACh. ACh facilitated or suppressed the visual responses of individual cells with a laminar bias: response suppression prevailed in layers 2/3, whereas response facilitation prevailed in layer 5. ACh effects on the stimulus contrast-response function showed that ACh changes the response gain upward or downward in facilitated or suppressed cells, respectively. Next, ACh effects on the signal-to-noise (S/N) ratio and the grating-phase information were tested. The grating-phase information was calculated as the F1/F0 ratio, which represents the amount of temporal response modulation at the fundamental frequency (F1) of a drifting grating relative to the mean evoked response (F0). In facilitated cells, ACh improved the S/N ratio, while in suppressed cells it enhanced the F1/F0 ratio without any concurrent reduction in the S/N ratio. These effects were predominantly observed in regular-spiking cells, but not in fast-spiking cells. Electrophysiological and histological findings suggest that ACh promotes the signaling of grating-phase information to higher-order areas by a suppressive effect on supragranular layers and enhances feedback signals with a high S/N ratio to subcortical areas by a facilitatory effect on infragranular layers. Thus, ACh distinctly and finely controls visual information processing in a manner that is specific for the modulation and cell type and is also laminar dependent.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology*
  • Action Potentials / drug effects*
  • Animals
  • Cholinergic Agonists / pharmacology
  • Electric Stimulation
  • Male
  • Neurons / classification
  • Neurons / drug effects*
  • Neurons / physiology
  • Photic Stimulation
  • Rats
  • Rats, Long-Evans
  • Visual Cortex / cytology
  • Visual Cortex / drug effects*
  • Visual Cortex / physiology
  • Visual Pathways / drug effects
  • Visual Pathways / physiology

Substances

  • Cholinergic Agonists
  • Acetylcholine

Grants and funding

This work was supported by KAKENHI, 21500369 to H. Sato, 22500573 to S. Shimegi, and 17021026, 20500285, 23135521 to H. Tamura. S. Soma was supported by the Japan Society for the Promotion of Science Research Fellowships. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.