title: Complete identification of four giant interneurons supplying mushroom body calyces in the cockroach Periplaneta americana.
abstract: Global inhibition is a fundamental physiological mechanism that has been proposed to shape odor representation in higher-order olfactory centers. A pair of mushroom bodies (MBs) in insect brains, an analog of the mammalian olfactory cortex, are implicated in multisensory integration and associative memory formation. With the use of single/multiple intracellular recording and staining in the cockroach Periplaneta americana, we succeeded in unambiguous identification of four tightly bundled GABA-immunoreactive giant interneurons that are presumably involved in global inhibitory control of the MB. These neurons, including three spiking neurons and one nonspiking neuron, possess dendrites in termination fields of MB output neurons and send axon terminals back to MB input sites, calyces, suggesting feedback roles onto the MB. The largest spiking neuron innervates almost exclusively the basal region of calyces, while the two smaller spiking neurons and the second-largest nonspiking neuron innervate more profusely the peripheral (lip) region of the calyces than the basal region. This subdivision corresponds well to the calycal zonation made by axon terminals of two populations of uniglomerular projection neurons with dendrites in distinct glomerular groups in the antennal lobe. The four giant neurons exhibited excitatory responses to every odor tested in a neuron-specific fashion, and two of the neurons also exhibited inhibitory responses in some recording sessions. Our results suggest that two parallel olfactory inputs to the MB undergo different forms of inhibitory control by the giant neurons, which may, in turn, be involved in different aspects of odor discrimination, plasticity, and state-dependent gain control. J. Comp. Neurol. 525:204-230, 2017. © 2016 Wiley Periodicals, Inc.
authors: Graduate School of Life Science, Hokkaido University, Sapporo, Japan.
authors: Naomi
authors: N
authors: Takahashi
authors: Graduate School of Life Science, Hokkaido University, Sapporo, Japan.
authors: Ko
authors: K
authors: Katoh
authors: Division of Biology, Department of Earth System Science, Fukuoka University, Fukuoka, Japan.
authors: Hidehiro
authors: H
authors: Watanabe
authors: Graduate School of Life Science, Hokkaido University, Sapporo, Japan.
authors: Yuta
authors: Y
authors: Nakayama
authors: Research Institute for Electronic Science, Hokkaido University, Sapporo, Japan.
authors: Masazumi
authors: M
authors: Iwasaki
authors: Faculty of Science, Hokkaido University, Sapporo, Japan.
authors: Makoto
authors: M
authors: Mizunami
authors: Research Institute for Electronic Science, Hokkaido University, Sapporo, Japan.
authors: Hiroshi
authors: H
authors: Nishino
mesh_terms: D000200:Action Potentials; D000818:Animals; D025461:Feedback, Physiological / Q000502:physiology; D021621:Imaging, Three-Dimensional; D007150:Immunohistochemistry; D007395:Interneurons / Q000166:cytology* / Q000502:physiology*; D008297:Male; D008839:Microelectrodes; D018613:Microscopy, Confocal; D024521:Mushroom Bodies / Q000166:cytology / Q000502:physiology; D009433:Neural Inhibition / Q000502:physiology; D009434:Neural Pathways / Q000166:cytology / Q000502:physiology; D010526:Periplaneta / Q000166:cytology* / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
chemical_list: D005680:gamma-Aminobutyric Acid
keywords: GABA; RRID: AB_477652; RRID: AB_528479; feedback; inhibition; intracellular recording; mushroom body; neoptera