Abstract

The navigational ability of birds has been a focus of popular and scientific interest for centuries, but relatively little is known about the neuronal networks that support avian navigation. In the brain, regions like the piriform cortex, olfactory bulbs, hippocampal formation, vestibular nuclei, and the wulst, are among the brain regions often discussed as involved in avian navigation. However, despite large literature showing a prominent role of some anterior and dorsal thalamic nuclei in mammalian spatial navigation, little is known about the role of the thalamus in avian navigation. Here, we analyzed a possible role of the dorsal anterior thalamic nuclei in avian navigation by combining olfactory manipulations during the transport of young homing pigeons to a release site and c-Fos immunohistochemistry for the mapping brain activity. The results reveal that odor modulated neurons in the avian dorsolateral lateral (DLL) subdivision of the anterior thalamic nuclei are actively involved in processing outward journey, navigational information. Outward journey information is used by pigeons to correctly determine the homeward direction. DLL participation in acquiring path-based information, and its modulation by olfactory exposure, broadens our understanding of the neural pathways underlying avian navigation.

Highlights

  • Spatial orientation underlies all aspects of animal behavior

  • The Avian Navigational Thalamus unfamiliar surroundings, can be used to help keep track of their path of movement (e.g., Papi and Casini, 1990; Patzke et al, 2010; reviewed in Wallraff, 2005); and (2) “Activation hypothesis” unfamiliar odors could function as an activator of neuronal circuits that process non-olfactory spatial information, i.e., nonhome odors could activate neuronal circuits that respond to and integrate navigational information from multiple sensory modalities (e.g., Jorge et al, 2009, 2010, 2014, 2016)

  • The findings reported here show, for the first time, that odor exposure in the context of homing differentially activates rostral dorsolateral neurons in the anterior thalamic nuclei and that these neurons seem to be sensitive to naturally occurring odors encountered during the outward journey when path-based information about geographic position is used to determine the homeward direction

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Summary

Introduction

Spatial orientation underlies all aspects of animal behavior. When exploring unfamiliar surroundings, many animals gather information about the path that they follow in order to keep track of their spatial position (Mittelstaedt and Mittelstaedt, 1980; Wiltschko and Wiltschko, 1982; Müller and Wehner, 1988; Bingman and Cheng, 2005; McNaughton et al, 2006). In a wide variety of animals atmospheric odors have been hypothesized to provide a major source of spatial information for long distance navigation (reviewed in Bingman and Cheng, 2005; Wallraff, 2005; Alerstam, 2006), but the role of olfactory cues in avian navigation remains controversial (Wiltschko, 1996; Freake et al, 2006; Jorge, 2011; Phillips and Jorge, 2014). In birds that are homing, olfactory input triggers higher levels of activity in the right olfactory bulb and left piriform cortex (but see Patzke et al, 2010)

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