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.

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

“…We identified type1 and type2 PNs based on their terminal zones in the calyces; terminal blebs of each type 1 PN are broadly distributed within zones III and IIIA of calyces, and those of each type2 PN are concentrated to the zone I (Strausfeld and Li, 1999a; Takahashi et al, 2017). In the current study, we intracellularly stained 115 type1 PNs, 63 type2 PNs, and 11 PNs of other types.…”

“…In the cockroach, KCs require convergent and synchronous inputs from multiple PNs for firing (Demmer and Kloppenburg, 2009). Additionally, inputs from PNs to KCs are modulated by four GABAergic calycal giant neurons (CGs) with dendrites in the termination fields of MB output neurons (Nishino et al, 2012b; Takahashi et al, 2017). Recent anatomical evidence suggests that olfactory inputs from type1 and type2 PNs to the MB calyces are modulated by different subset of CGs (Takahashi et al, 2017).…”

“…Additionally, inputs from PNs to KCs are modulated by four GABAergic calycal giant neurons (CGs) with dendrites in the termination fields of MB output neurons (Nishino et al, 2012b; Takahashi et al, 2017). Recent anatomical evidence suggests that olfactory inputs from type1 and type2 PNs to the MB calyces are modulated by different subset of CGs (Takahashi et al, 2017). Specifically, the axon terminal of three CGs, including a non-spiking neuron, are found to converge on the terminal region of type2 PNs, forming fine and complex negative-feedback circuits.…”

Circuit and cellular mechanisms facilitate the transformation from dense to sparse coding in the insect olfactory system

“…Animals are required to rapidly identify behaviorally relevant stimulus features in a rich 29 and dynamic sensory environment, and neural computation in sensory pathways is tailored 30 to this need. Sparse stimulus encoding has been identified as an essential feature of sensory 31 processing in higher brain areas in both, invertebrate [1,2,3,4, 5] and vertebrate [6, 7, 8, 9] 32 systems. Sparse representations provide an economical means of neural information coding 33 [10,11] where information is represented by only a small fraction of all neurons (popula-34 tion sparseness) and each activated neuron generates only few action potentials (temporal 35 sparseness) for a highly specific stimulus configuration (lifetime sparseness).…”

“…Both LNs and PNs receive direct ORN input. We tuned synaptic weights of the 94 model to match physiologically observed firing rates of PNs and LNs, which are both about 95 8 Hz [1,42,43] (for details see Methods). Lateral inhibition and spike-frequency adaptation, 96 the neural mechanisms under investigation, both provide an inhibitory contribution to a 97 neuron's total input.…”