Descending Control in a Locomotor System

Locomotion is highly variable because it needs to adapt to a wide range of behavioral contexts. Consequently, the motor output and the underlying neuronal circuits need to be adapted in order to fit into the environmental circumstances, e.g. modulated in terms of speed, strength, or direction. Most importantly, locomotion needs to be initiated to generate necessary movements and under different circumstances it needs to be terminated. It was shown in a broad range of animals, both vertebrates and invertebrates, that motor output is controlled by descending information that arise outside of the locomotor systems. In the central nervous systems (CNS) of vertebrates these information are provided by distinct neuronal groups that comprise large numbers of neurons. In invertebrate CNSs, however, the smaller number of neurons had led to the discovery of individual neurons that possess the ability to initiated or terminate complex behaviors. The swimmeret system of crayfish is a well characterized system to investigate the neuronal mechanisms underlying locomotion and coordination of multiple pairs of limbs. It consists of four paired limbs on the animal’s abdomen that perform cycles of alternating power and return stroke movements when the crayfish swims. On the one hand, the neuronal network that generates these movements was investigated in great detail. The activity of each limb is driven by two classes of interneurons which form the central pattern generator (CPG). On the other hand, descending command neurons were found that initiate or terminate fictive locomotion in the isolated swimmeret system. However, the question of how these neurons affect the CPGs of the swimmeret system remained unanswered. In order to address this question, I stimulated separated axon bundles within the abdominal nerve cord and performed extracellular and intracellular recordings of the swimmeret system’s activity. I successfully showed that my stimulations recruited individual command neurons that affected fictive locomotion in terms of initiation and termination. Interestingly, I was able to show that excitatory command neurons can accelerate and strengthen fictive locomotion. While acceleration is implemented bilaterally, strengthening of the motor output contains a side-specific component. I further demonstrated that only one class of CPG neurons is directly targeted by descending excitatory input. Furthermore, the CPGs are unilaterally targeted which may reflect a mechanism to initiate a specific behavior, e.g. turning. This is the first evidence of how descending input modulates the swimmeret system’s motor output and gives new insights into the general control of locomotion

GABAergic modulation of olfactomotor transmission in lampreys.

Odor-guided behaviors, including homing, predator avoidance, or food and mate searching, are ubiquitous in animals. It is only recently that the neural substrate underlying olfactomotor behaviors in vertebrates was uncovered in lampreys. It consists of a neural pathway extending from the medial part of the olfactory bulb (medOB) to locomotor control centers in the brainstem via a single relay in the caudal diencephalon. This hardwired olfactomotor pathway is present throughout life and may be responsible for the olfactory-induced motor behaviors seen at all life stages. We investigated modulatory mechanisms acting on this pathway by conducting anatomical (tract tracing and immunohistochemistry) and physiological (intracellular recordings and calcium imaging) experiments on lamprey brain preparations. We show that the GABAergic circuitry of the olfactory bulb (OB) acts as a gatekeeper of this hardwired sensorimotor pathway. We also demonstrate the presence of a novel olfactomotor pathway that originates in the non-medOB and consists of a projection to the lateral pallium (LPal) that, in turn, projects to the caudal diencephalon and to the mesencephalic locomotor region (MLR). Our results indicate that olfactory inputs can induce behavioral responses by activating brain locomotor centers via two distinct pathways that are strongly modulated by GABA in the OB. The existence of segregated olfactory subsystems in lampreys suggests that the organization of the olfactory system in functional clusters may be a common ancestral trait of vertebrates