Abstract

Cockroaches are scavengers that forage through dark, maze-like environments. Like other foraging animals, for instance rats, they must continually asses their situation to keep track of targets and negotiate barriers. While navigating a complex environment, all animals need to integrate sensory information in order to produce appropriate motor commands. The integrated sensory cues can be used to provide the animal with an environmental and contextual reference frame for the behavior. To successfully reach a goal location, navigational cues continuously derived from sensory inputs have to be utilized in the spatial guidance of motor commands. The sensory processes, contextual and spatial mechanisms, and motor outputs contributing to navigation have been heavily studied in rats. In contrast, many insect studies focused on the sensory and/or motor components of navigation, and our knowledge of the abstract representation of environmental context and spatial information in the insect brain is relatively limited. Recent reports from several laboratories have explored the role of the central complex (CX), a sensorimotor region of the insect brain, in navigational processes by recording the activity of CX neurons in freely-moving insects and in more constrained, experimenter-controlled situations. The results of these studies indicate that the CX participates in processing the temporal and spatial components of sensory cues, and utilizes these cues in creating an internal representation of orientation and context, while also directing motor control. Although these studies led to a better understanding of the CX's role in insect navigation, there are still major voids in the literature regarding the underlying mechanisms and brain regions involved in spatial navigation. The main goal of this review is to place the above listed findings in the wider context of animal navigation by providing an overview of the neural mechanisms of navigation in rats and summarizing and comparing our current knowledge on the CX's role in insect navigation to these processes. By doing so, we aimed to highlight some of the missing puzzle pieces in insect navigation and provide a different perspective for future directions.

Highlights

  • Insects are by just about any measure the most successful animal group inhabiting almost every conceivable niche on the planet

  • Their similar ecology and foraging behaviors indicate that the two model organisms likely depend on the same sensory cues and similar integration processes to orient themselves, we predict that there might be some similarities between the circuits underlying navigation

  • We further extended the results from the fly experiments by adopting some of the classical methods used in rat head direction cell studies and applying them in our experiments on cockroach CX function (Varga and Ritzmann, 2016)

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Summary

INTRODUCTION

Insects are by just about any measure the most successful animal group inhabiting almost every conceivable niche on the planet. Large amounts of neuromodulatory receptors and targets have been identified (Kahsai and Winther, 2011; Boyan and Liu, 2016) and motor control effects demonstrated (Bender et al, 2010; Martin et al, 2015) These studies combine to suggest that the CX plays a pivotal role in guiding appropriate behaviors for each species and adjusting the accompanying movements to match the current context that an individual insect finds itself in at any point in time. One reason for focusing on cockroaches is that they occupy an ecological niche similar to rat habitats, which are a major model for mammalian navigation Both rats and cockroaches are scavengers that forage in darkened environments and often navigate in complex, maze-like burrows (Roth and Willis, 1960; Feng and Himsworth, 2014). We will describe findings in our laboratory and others that suggest that the CX is involved in this kind of navigation but begin to outline what that role might be

SENSORY INPUTS TO THE CX
WHAT CAN WE LEARN FROM RAT NAVIGATION STUDIES?
HIPPOCAMPAL FORMATION AND RELATED CIRCUITS
SPATIAL CODE IN THE BASAL GANGLIA
THE NEURAL SUBSTRATES OF NAVIGATION IN THE CX
MOTOR CONTROL FROM THE CX
CONCLUSIONS
AUTHOR CONTRIBUTIONS
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