Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach.

Hidehiro Watanabe,Hiroshi Nishino,Makoto Mizunami,Fumio Yokohari

doi:10.3389/fncir.2017.00032

Hidehiro Watanabe, Hiroshi Nishino + Show 2 more

Open Access

https://doi.org/10.3389/fncir.2017.00032

Copy DOI

Abstract

In animals, sensory processing via parallel pathways, including the olfactory system, is a common design. However, the mechanisms that parallel pathways use to encode highly complex and dynamic odor signals remain unclear. In the current study, we examined the anatomical and physiological features of parallel olfactory pathways in an evolutionally basal insect, the cockroach Periplaneta americana. In this insect, the entire system for processing general odors, from olfactory sensory neurons to higher brain centers, is anatomically segregated into two parallel pathways. Two separate populations of secondary olfactory neurons, type1 and type2 projection neurons (PNs), with dendrites in distinct glomerular groups relay olfactory signals to segregated areas of higher brain centers. We conducted intracellular recordings, revealing olfactory properties and temporal patterns of both types of PNs. Generally, type1 PNs exhibit higher odor-specificities to nine tested odorants than type2 PNs. Cluster analyses revealed that odor-evoked responses were temporally complex and varied in type1 PNs, while type2 PNs exhibited phasic on-responses with either early or late latencies to an effective odor. The late responses are 30–40 ms later than the early responses. Simultaneous intracellular recordings from two different PNs revealed that a given odor activated both types of PNs with different temporal patterns, and latencies of early and late responses in type2 PNs might be precisely controlled. Our results suggest that the cockroach is equipped with two anatomically and physiologically segregated parallel olfactory pathways, which might employ different neural strategies to encode odor information.

Highlights

Information processing along parallel pathways is a common feature of animal sensory systems, enabling fast and reliable representations of highly complex and dynamic sensory information
Axons of uniglomerular projection neurons (PNs) run through the medial ALT (m-ALT) and nearby tracts (ALT-2 and ALT-3), and terminate in the medial and lateral calyces (CA) of the mushroom bodies (MBs) first and in the lateral horns (LHs) (Malun et al, 1993; Strausfeld and Li, 1999a; Nishino et al, 2012a)
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)

Summary

Introduction

Information processing along parallel pathways is a common feature of animal sensory systems, enabling fast and reliable representations of highly complex and dynamic sensory information. Parallel sensory pathways typically extract and process different types of stimulus parameters. In the vertebrate olfactory system, general and pheromonal odors are processed in the main olfactory and vomeronasal pathways, respectively (Tirindelli et al, 2009). Within the main olfactory pathway, mitral and tufted cells in the olfactory bulb process odor qualities and timing information, respectively (Nagayama et al, 2004; Igarashi et al, 2012). Olfactory sensory neurons (OSNs) are housed in the antennal sensilla and project to glomeruli in the AL. A large number of OSNs, which express a cognate type of odorant receptor relay onto a moderate number of secondary olfactory interneurons, projection neurons (PNs), and local interneurons (LNs). LNs in the AL interconnect glomeruli and contribute to odor-induced spatiotemporal activity patterns of PNs (Wilson et al, 2004; Watanabe et al, 2012a)

Methods

Results

Conclusion