Functional morphology of the primary olfactory centers in the brain of the hermit crab Coenobita clypeatus (Anomala, Coenobitidae)

Marta A Polanska,Tina Kirchhoff,Steffen Harzsch,Bill S Hansson,Heinrich Dircksen

doi:10.1007/s00441-020-03199-5

Abstract

Terrestrial hermit crabs of the genus Coenobita display strong behavioral responses to volatile odors and are attracted by chemical cues of various potential food sources. Several aspects of their sense of aerial olfaction have been explored in recent years including behavioral aspects and structure of their peripheral and central olfactory pathway. Here, we use classical histological methods and immunohistochemistry against the neuropeptides orcokinin and allatostatin as well as synaptic proteins and serotonin to provide insights into the functional organization of their primary olfactory centers in the brain, the paired olfactory lobes. Our results show that orcokinin is present in the axons of olfactory sensory neurons, which target the olfactory lobe. Orcokinin is also present in a population of local olfactory interneurons, which may relay lateral inhibition across the array of olfactory glomeruli within the lobes. Extensive lateral connections of the glomeruli were also visualized using the histological silver impregnation method according to Holmes-Blest. This technique also revealed the structural organization of the output pathway of the olfactory system, the olfactory projection neurons, the axons of which target the lateral protocerebrum. Within the lobes, the course of their axons seems to be reorganized in an axon-sorting zone before they exit the system. Together with previous results, we combine our findings into a model on the functional organization of the olfactory system in these animals.

Highlights

Multiple times during their evolutionary radiation, representatives of several malacostracan taxa have independently invaded the terrestrial habitat
Immunohistochemistry against presynaptic vesicle proteins to label synapse-dense areas reveals an array of wedge-shaped synaptic units, which are radially arranged around a nonsynaptic fibrous core (FC; Fig. 2a, b)
An additional array of parallel fibers can be recognized in the center of the fibrous core, which we will term “central projection neuron hub” in accordance with the terminology established by Ito et al (2014), and which we will describe in more detail below

Summary

Introduction

Multiple times during their evolutionary radiation, representatives of several malacostracan taxa have independently invaded the terrestrial habitat. The glomeruli typically are regionalized into functional compartments along their long axis, and in representatives of the crayfish (Blaustein et al 1988; Sandeman and Luff 1973), clawed lobsters (Langworthy et al 1997), spiny lobsters (Blaustein et al 1988; Schmidt and Ache 1992, 1996, 1997; Wachowiak and Ache 1997; Wachowiak et al 1997), and hermit crabs (Harzsch and Hansson 2008; Krieger et al 2010, 2012), an outer cap, a subcap, and a base region can be distinguished This compartmentalization, which is mirrored in the glomerular neurochemistry (Langworthy et al 1997; Schmidt and Ache 1997; Polanska et al 2012), suggests that complex local processing occurs at the level of single glomeruli. Another type of olfactory interneurons, the projection neurons, represent the output pathway of the system, and their axons assemble in the projection neuron tract to target specific protocerebral areas

Methods

Results

Conclusion