Abstract

Author SummaryAnimal behaviors, including locomotion, can be driven by olfactory cues, such as pheromones or food sources. The neural substrate (neuroanatomical connections and physiological signals) that permits the transformation of olfactory inputs into locomotor responses is still unknown in vertebrates. In the present study, we identify such a neural substrate in the lamprey. Here, olfactory signals from the outside world are transmitted to the reticulospinal neurons in the lower brainstem, which provide the descending locomotor command to the spinal cord. We found that this circuit originates in the medial portion of the olfactory bulb and that connections are made in the posterior tuberculum, a ventral diencephalic structure. These inputs are then conveyed to the mesencephalic locomotor region, known to project extensively to brainstem reticulospinal neurons and thereby activate locomotion. Our results illuminate a specific dedicated neural substrate in the brain of lampreys that underlies olfactory-motor responses, which is activated by both food-related or pheromonal olfactory cues. It will be of interest to determine whether such a pathway is preserved in all vertebrates.

Highlights

  • Animals use olfaction in different behavioral contexts such as food seeking, social communication, and reproduction

  • Olfactory signals from the outside world are transmitted to the reticulospinal neurons in the lower brainstem, which provide the descending locomotor command to the spinal cord. We found that this circuit originates in the medial portion of the olfactory bulb and that connections are made in the posterior tuberculum, a ventral diencephalic structure

  • Excitatory responses to odors and pheromones were observed in RS cells of both females and males

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Summary

Introduction

Animals use olfaction in different behavioral contexts such as food seeking, social communication, and reproduction. Motor behaviors, including locomotion, can be generated by olfactory stimulation in several species of vertebrates, including fishes [1], rats [2], humans [3], and lampreys [4]. The RS cells receive inputs from the periphery, the spinal cord, and locomotor centers in the forebrain and brainstem, including the mesencephalic locomotor region (MLR [19,20,21]), a highly conserved neural center controlling locomotion in all vertebrate species. Another locomotor center located in the diencephalon has been described in lampreys [22].

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