title: Curtailing effect of awakening on visual responses of cortical neurons by cholinergic activation of inhibitory circuits.
abstract: Visual responsiveness of cortical neurons changes depending on the brain state. Neural circuit mechanism underlying this change is unclear. By applying the method of in vivo two-photon functional calcium imaging to transgenic rats in which GABAergic neurons express fluorescent protein, we analyzed changes in visual response properties of cortical neurons when animals became awakened from anesthesia. In the awake state, the magnitude and reliability of visual responses of GABAergic neurons increased whereas the decay of responses of excitatory neurons became faster. To test whether the basal forebrain (BF) cholinergic projection is involved in these changes, we analyzed effects of electrical and optogenetic activation of BF on visual responses of mouse cortical neurons with in vivo imaging and whole-cell recordings. Electrical BF stimulation in anesthetized animals induced the same direction of changes in visual responses of both groups of neurons as awakening. Optogenetic activation increased the frequency of visually evoked action potentials in GABAergic neurons but induced the delayed hyperpolarization that ceased the late generation of action potentials in excitatory neurons. Pharmacological analysis in slice preparations revealed that photoactivation-induced depolarization of layer 1 GABAergic neurons was blocked by a nicotinic receptor antagonist, whereas non-fast-spiking layer 2/3 GABAergic neurons was blocked only by the application of both nicotinic and muscarinic receptor antagonists. These results suggest that the effect of awakening is mediated mainly through nicotinic activation of layer 1 GABAergic neurons and mixed nicotinic/muscarinic activation of layer 2/3 non-fast-spiking GABAergic neurons, which together curtails the visual responses of excitatory neurons.
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan.
authors: Rui
authors: R
authors: Kimura
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan.
authors: Mir-Shahram
authors: MS
authors: Safari
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan, Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran.
authors: Javad
authors: J
authors: Mirnajafi-Zadeh
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan.
authors: Rie
authors: R
authors: Kimura
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan.
authors: Teppei
authors: T
authors: Ebina
authors: CREST, Japan Science and Technology Agency, Tokyo 102-0075, Japan, Gunma University Graduate School of Medicine, Maebashi 371-8511 Japan, and.
authors: Yuchio
authors: Y
authors: Yanagawa
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan, PRESTO, Japan Science and Technology Agency, Tokyo 102-0075, Japan tsumoto@brain.riken.jp sohya@brain.riken.jp.
authors: Kazuhiro
authors: K
authors: Sohya
authors: Brain Science Institute, RIKEN, Wako 351-0198 Japan, tsumoto@brain.riken.jp sohya@brain.riken.jp.
authors: Tadaharu
authors: T
authors: Tsumoto
mesh_terms: D000818:Animals; D002540:Cerebral Cortex / Q000502:physiology*; D005074:Evoked Potentials, Visual / Q000502:physiology*; D005260:Female; D008297:Male; D051379:Mice; D008822:Mice, Transgenic; D009415:Nerve Net / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009924:Organ Culture Techniques; D016548:Prosencephalon / Q000378:metabolism / Q000502:physiology; D051381:Rats; D055647:Rats, Transgenic; D050495:Vesicular Inhibitory Amino Acid Transport Proteins / Q000378:metabolism* / Q000502:physiology; D014851:Wakefulness / Q000502:physiology*
chemical_list: D050495:Vesicular Inhibitory Amino Acid Transport Proteins
keywords: GABAergic interneuron; brain state; cholinergic projection; transgenic rat; two-photon functional Ca2+ imaging; visual cortex