Olfactory Projections to Locomotor Control Centers in the Sea Lamprey.

Although olfaction is well known to guide animal behavior, the neural circuits underlying the motor responses elicited by olfactory inputs are poorly understood. In the sea lamprey, anatomical evidence shows that olfactory inputs project to the posterior tuberculum (PT), a structure containing dopaminergic (DA) neurons homologous to the mammalian ventral tegmental area and the substantia nigra pars compacta. Olfactory inputs travel directly from the medial olfactory bulb (medOB) or indirectly through the main olfactory bulb and the lateral pallium (LPal).

The distribution and chemosensory responses of pharyngeal taste buds in the sea lamprey Petromyzon marinus.

Little is known about the chemosensory system of gustation in sea lampreys, basal jawless vertebrates that feed voraciously on live prey. The objective of this study was to investigate taste bud distribution and chemosensory responses along the length of the pharynx in the sea lamprey. Scanning electron microscopy and immunocytochemistry revealed taste buds and associated axons at all six lateral pharyngeal locations between the seven pairs of internal gill pores.

Revisiting the two rhythm generators for respiration in lampreys.

In lampreys, respiration consists of a fast and a slow rhythm. This study was aimed at characterizing both anatomically and physiologically the brainstem regions involved in generating the two rhythms. The fast rhythm generator has been located by us and others in the rostral hindbrain, rostro-lateral to the trigeminal motor nucleus.

Dopamine control of downstream motor centers.

The role of dopamine in the control of movement is traditionally associated with ascending projections to the basal ganglia. However, more recently descending dopaminergic pathways projecting to downstream brainstem motor circuits were discovered. In lampreys, salamanders, and rodents, these include projections to the downstream Mesencephalic Locomotor Region (MLR), a brainstem region controlling locomotion.

The mesencephalic locomotor region recruits V2a reticulospinal neurons to drive forward locomotion in larval zebrafish.

The mesencephalic locomotor region (MLR) is a brain stem area whose stimulation triggers graded forward locomotion. How MLR neurons recruit downstream vsx2 (V2a) reticulospinal neurons (RSNs) is poorly understood. Here, to overcome this challenge, we uncovered the locus of MLR in transparent larval zebrafish and show that the MLR locus is distinct from the nucleus of the medial longitudinal fasciculus.

Locomotor pattern generation and descending control: a historical perspective.

The ability to generate and control locomotor movements depends on complex interactions between many areas of the nervous system, the musculoskeletal system, and the environment. How the nervous system manages to accomplish this task has been the subject of investigation for more than a century. In vertebrates, locomotion is generated by neural networks located in the spinal cord referred to as central pattern generators.

Brainstem neural mechanisms controlling locomotion with special reference to basal vertebrates.

Over the last 60 years, the basic neural circuitry responsible for the supraspinal control of locomotion has progressively been uncovered. Initially, significant progress was made in identifying the different supraspinal structures controlling locomotion in mammals as well as some of the underlying mechanisms. It became clear, however, that the complexity of the mammalian central nervous system (CNS) prevented researchers from characterizing the detailed cellular mechanisms involved and that animal models with a simpler nervous system were needed.

Cholinergic Modulation of Locomotor Circuits in Vertebrates.

Locomotion is a basic motor act essential for survival. Amongst other things, it allows animals to move in their environment to seek food, escape predators, or seek mates for reproduction. The neural mechanisms involved in the control of locomotion have been examined in many vertebrate species and a clearer picture is progressively emerging.

Olfactory-induced locomotion in lampreys.

The olfactory system allows animals to navigate in their environment to feed, mate, and escape predators. It is well established that odorant exposure or electrical stimulation of the olfactory system induces stereotyped motor responses in fishes. However, the neural circuitry responsible for the olfactomotor transformations is only beginning to be unraveled.

Descending Dopaminergic Inputs to Reticulospinal Neurons Promote Locomotor Movements.

Meso-diencephalic dopaminergic neurons are known to modulate locomotor behaviors through their ascending projections to the basal ganglia, which in turn project to the mesencephalic locomotor region, known to control locomotion in vertebrates. In addition to their ascending projections, dopaminergic neurons were found to increase locomotor movements through direct descending projections to the mesencephalic locomotor region and spinal cord. Intriguingly, fibers expressing tyrosine hydroxylase (TH), the rate-limiting enzyme of dopamine synthesis, were also observed around reticulospinal neurons of lampreys.

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): II. Ontogeny and immunocytochemical characterization of solitary chemosensory cells.

Solitary chemosensory cells (SCCs) and their innervating fibers are located in the respiratory system of many vertebrates, including papillae on lamprey gill pores. In order to gain stronger insight for the role of these chemosensory cells, we examined immunocytochemical and innervation characteristics, as well as abundance at the different stages of the lamprey life cycle. The SCCs were distinguished from the surrounding epithelial cells by calretinin and phospholipase C140 immunoreactivity.

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): I. Neuroanatomy and physiology.

Molecules present in an animal's environment can indicate the presence of predators, food, or sexual partners and consequently, induce migratory, reproductive, foraging, or escape behaviors. Three sensory systems, the olfactory, gustatory, and solitary chemosensory cell (SCC) systems detect chemical stimuli in vertebrates. While a great deal of research has focused on the olfactory and gustatory system over the years, it is only recently that significant attention has been devoted to the SCC system.

Dopaminergic modulation of olfactory-evoked motor output in sea lampreys (Petromyzon marinus L.).

Detection of chemical cues is important to guide locomotion in association with feeding and sexual behavior. Two neural pathways responsible for odor-evoked locomotion have been characterized in the sea lamprey (Petromyzon marinus L.), a basal vertebrate.

A Brainstem Neural Substrate for Stopping Locomotion.

Locomotion occurs sporadically and needs to be started, maintained, and stopped. The neural substrate underlying the activation of locomotion is partly known, but little is known about mechanisms involved in termination of locomotion. Recently, reticulospinal neurons (stop cells) were found to play a crucial role in stopping locomotion in the lamprey: their activation halts ongoing locomotion and their inactivation slows down the termination process.

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.

Nigral Glutamatergic Neurons Control the Speed of Locomotion.

The mesencephalic locomotor region (MLR) plays a crucial role in locomotor control. In vertebrates, stimulation of the MLR at increasing intensities elicits locomotion of growing speed. This effect has been presumed to result from higher brain inputs activating the MLR like a dimmer switch.

Dopamine and the Brainstem Locomotor Networks: From Lamprey to Human.

In vertebrates, dopamine neurons are classically known to modulate locomotion via their ascending projections to the basal ganglia that project to brainstem locomotor networks. An increased dopaminergic tone is associated with increase in locomotor activity. In pathological conditions where dopamine cells are lost, such as in Parkinson's disease, locomotor deficits are traditionally associated with the reduced ascending dopaminergic input to the basal ganglia.

Odorant organization in the olfactory bulb of the sea lamprey.

Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labelling established that lateral and dorsal bulbar territories receive the axons of sensory neurons broadly distributed in the main olfactory epithelium and that the medial region receives sensory neuron input only from neurons projecting from the accessory olfactory organ.

The neural control of respiration in lampreys.

This review focuses on past and recent findings that have contributed to characterize the neural networks controlling respiration in the lamprey, a basal vertebrate. As in other vertebrates, respiration in lampreys is generated centrally in the brainstem. It is characterized by the presence of a fast and a slow respiratory rhythm.

A Specific Population of Reticulospinal Neurons Controls the Termination of Locomotion.

Locomotion requires the proper sequencing of neural activity to start, maintain, and stop it. Recently, brainstem neurons were shown to specifically stop locomotion in mammals. However, the cellular properties of these neurons and their activity during locomotion are still unknown.

A descending dopamine pathway conserved from basal vertebrates to mammals.

Dopamine neurons are classically known to modulate locomotion indirectly through ascending projections to the basal ganglia that project down to brainstem locomotor networks. Their loss in Parkinson's disease is devastating. In lampreys, we recently showed that brainstem networks also receive direct descending dopaminergic inputs that potentiate locomotor output.

Sensory Activation of Command Cells for Locomotion and Modulatory Mechanisms: Lessons from Lampreys.

Sensorimotor transformation is one of the most fundamental and ubiquitous functions of the central nervous system (CNS). Although the general organization of the locomotor neural circuitry is relatively well understood, less is known about its activation by sensory inputs and its modulation. Utilizing the lamprey model, a detailed understanding of sensorimotor integration in vertebrates is emerging.

The mesencephalic locomotor region sends a bilateral glutamatergic drive to hindbrain reticulospinal neurons in a tetrapod.

In vertebrates, stimulation of the mesencephalic locomotor region (MLR) on one side evokes symmetrical locomotor movements on both sides. How this occurs was previously examined in detail in a swimmer using body undulations (lamprey), but in tetrapods the downstream projections from the MLR to brainstem neurons are not fully understood. Here we examined the brainstem circuits from the MLR to identified reticulospinal neurons in the salamander Notophthalmus viridescens.

Testing the evolutionary conservation of vocal motoneurons in vertebrates.

Medullary motoneurons drive vocalization in many vertebrate lineages including fish, amphibians, birds, and mammals. The developmental history of vocal motoneuron populations in each of these lineages remains largely unknown. The highly conserved transcription factor Paired-like Homeobox 2b (Phox2b) is presumed to be expressed in all vertebrate hindbrain branchial motoneurons, including laryngeal motoneurons essential for vocalization in humans.

The neuroanatomical organization of projection neurons associated with different olfactory bulb pathways in the sea lamprey, Petromyzon marinus.

Although there is abundant evidence for segregated processing in the olfactory system across vertebrate taxa, the spatial relationship between the second order projection neurons (PNs) of olfactory subsystems connecting sensory input to higher brain structures is less clear. In the sea lamprey, there is tight coupling between olfaction and locomotion via PNs extending to the posterior tuberculum from the medial region of the olfactory bulb. This medial region receives peripheral input predominantly from the accessory olfactory organ.