A lamprey neural cell type atlas illuminates the origins of the vertebrate brain.

The vertebrate brain emerged more than ~500 million years ago in common evolutionary ancestors. To systematically trace its cellular and molecular origins, we established a spatially resolved cell type atlas of the entire brain of the sea lamprey-a jawless species whose phylogenetic position affords the reconstruction of ancestral vertebrate traits-based on extensive single-cell RNA-seq and in situ sequencing data. Comparisons of this atlas to neural data from the mouse and other jawed vertebrates unveiled various shared features that enabled the reconstruction of cell types, tissue structures and gene expression programs of the ancestral vertebrate brain.

Expression of Kisspeptin 1 in the Brain of the Adult Sea Lamprey .

Kisspeptin peptides play major roles in the regulation of reproduction and puberty onset in mammals. While most mammals only have one kisspeptin gene, other jawed vertebrates present two or three genes. Recent data also revealed the presence of two genes in lampreys (jawless vertebrates).

Inhibition of Gamma-Secretase Promotes Axon Regeneration After a Complete Spinal Cord Injury.

In a recent study, we showed that GABA and baclofen (a GABAB receptor agonist) inhibit caspase activation and promote axon regeneration in descending neurons of the sea lamprey brainstem after a complete spinal cord injury (Romaus-Sanjurjo et al., 2018a). Now, we repeated these treatments and performed 2 independent Illumina RNA-Sequencing studies in the brainstems of control and GABA or baclofen treated animals.

Differential expression of five prosomatostatin genes in the central nervous system of the catshark Scyliorhinus canicula.

Five prosomatostatin genes (PSST1, PSST2, PSST3, PSST5, and PSST6) have been recently identified in elasmobranchs (Tostivint et al., General and Comparative Endocrinology, 2019, 279, 139-147). In order to gain insight into the contribution of each somatostatin to specific nervous systems circuits and behaviors in this important jawed vertebrate group, we studied the distribution of neurons expressing PSST mRNAs in the central nervous system (CNS) of Scyliorhinus canicula using in situ hybridization.

Data on the recovery of glycinergic neurons after spinal cord injury in lampreys.

We used immunohistochemical methods to quantify changes in the number of glycine-immunoreactive neurons of the dorsomedial, lateral and cerebrospinal fluid contacting cell populations of the spinal cord of larval sea lampreys after a complete spinal cord injury. The data presented here are quantifications of the number of glycine-immunoreactive neurons located in the rostral and caudal stumps of the spinal cord and the corresponding statistical analyses. These data show that, glycine immunoreactivity is lost in glycinergic neurons immediately after injury and that the number of glycine-immunoreactive neurons is recovered in the following two weeks.

Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey .

Galanin is a neuropeptide that is widely expressed in the mammalian brain, where it regulates many physiological processes, including feeding and nociception. Galanin has been characterized extensively in jawed vertebrates (gnathostomes), but little is known about the galanin system in the most ancient extant vertebrate class, the jawless vertebrates or agnathans. Here, we identified and cloned a cDNA encoding the sea lamprey () galanin precursor ().

Taurine Promotes Axonal Regeneration after a Complete Spinal Cord Injury in Lampreys.

Taurine is one of the most abundant free amino acids in the brain. It is well known that taurine protects the brain from further damage after a traumatic event. However, only a few studies have looked at the possible role of taurine in the regulation of axon regeneration after injury.

Serotonin inhibits axonal regeneration of identifiable descending neurons after a complete spinal cord injury in lampreys.

Classical neurotransmitters are mainly known for their roles as neuromodulators, but they also play important roles in the control of developmental and regenerative processes. Here, we used the lamprey model of spinal cord injury to study the effect of serotonin in axon regeneration at the level of individually identifiable descending neurons. Pharmacological and genetic manipulations after a complete spinal cord injury showed that endogenous serotonin inhibits axonal regeneration in identifiable descending neurons through the activation of serotonin 1A receptors and a subsequent decrease in cyclic adenosine monophosphate (cAMP) levels.

Data on the effect of a muscimol treatment in caspase activation in descending neurons of lampreys after a complete spinal cord injury.

In this article, caspase activation in identifiable reticulospinal neurons of lampreys was inhibited after a complete spinal cord injury using a specific agonist of the GABAA receptor (muscimol). The data presented in this article are quantifications of fluorescent labelling of identifiable descending neurons of larval lampreys after a complete spinal cord injury using fluorochrome-labelled inhibitors of caspases (FLICA) and the corresponding statistical analysis. A single dose of muscimol decreased the intensity of FLICA labelling in giant identifiable reticulospinal neurons following spinal cord injury in lampreys.

GABA promotes survival and axonal regeneration in identifiable descending neurons after spinal cord injury in larval lampreys.

The poor regenerative capacity of descending neurons is one of the main causes of the lack of recovery after spinal cord injury (SCI). Thus, it is of crucial importance to find ways to promote axonal regeneration. In addition, the prevention of retrograde degeneration leading to the atrophy/death of descending neurons is an obvious prerequisite to activate axonal regeneration.

Cloning of the GABA Receptor Subunits B1 and B2 and their Expression in the Central Nervous System of the Adult Sea Lamprey.

In vertebrates, γ-aminobutyric acid (GABA) is the main inhibitory transmitter in the central nervous system (CNS) acting through ionotropic (GABA) and metabotropic (GABA) receptors. The GABA receptor produces a slow inhibition since it activates second messenger systems through the binding and activation of guanine nucleotide-binding proteins [G-protein-coupled receptors (GPCRs)]. Lampreys are a key reference to understand molecular evolution in vertebrates.

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys.

Lampreys recover locomotion following a spinal cord injury (SCI). Glutamate is necessary to initiate and control locomotion and recent data suggest a crucial role for intraspinal neurons in functional recovery following SCI. We aimed to determine whether, in lampreys, axotomized spinal glutamatergic neurons, which lose glutamate immunoreactivity immediately after SCI, recover it later on and to study the long-term evolution and anatomical recovery of the spinal glutamatergic system after SCI.

Identification of three somatostatin genes in lampreys.

Somatostatins (SSs) are a structurally diverse family of neuropeptides that play important roles in the regulation of growth, development and metabolism in vertebrates. It has been recently proposed that the common ancestor of gnathostomes possessed three SS genes, namely SS1, SS2 and SS5. SS1 and SS2 are still present in most extant gnathostome species investigated so far while SS5 primarily occurs in chondrichthyes, actinopterygians and actinistia but not in tetrapods.

Spatiotemporal Pattern of Doublecortin Expression in the Retina of the Sea Lamprey.

Despite the importance of doublecortin (DCX) for the development of the nervous system, its expression in the retina of most vertebrates is still unknown. The key phylogenetic position of lampreys, together with their complex life cycle, with a long blind larval stage and an active predator adult stage, makes them an interesting model to study retinal development. Here, we studied the spatiotemporal pattern of expression of DCX in the retina of the sea lamprey.

Tryptophan hydroxylase and serotonin receptor 1A expression in the retina of the sea lamprey.

The dual development of the retina of lampreys is exceptional among vertebrates and offers an interesting EvoDevo (evolutionary developmental biology) model for understanding the origin and evolution of the vertebrate retina. Only a single type of photoreceptor, ganglion cell and bipolar cell are present in the early-differentiated central retina of lamprey prolarvae. A lateral retina appears later in medium-sized larvae (about 3 years after hatching in the sea lamprey), growing and remaining largely neuroblastic until metamorphosis.

Full anatomical recovery of the dopaminergic system after a complete spinal cord injury in lampreys.

Following a spinal injury, lampreys at first are paralyzed below the level of transection. However, they recover locomotion after several weeks, and this is accompanied by the regeneration of descending axons from the brain and the production of new neurons in the spinal cord. Here, we aimed to analyse the changes in the dopaminergic system of the sea lamprey after a complete spinal transection by studying the changes in dopaminergic cell numbers and dopaminergic innervation in the spinal cord.

The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain.

Left-right asymmetries in the epithalamic region of the brain are widespread across vertebrates, but their magnitude and laterality varies among species. Whether these differences reflect independent origins of forebrain asymmetries or taxa-specific diversifications of an ancient vertebrate feature remains unknown. Here we show that the catshark Scyliorhinus canicula and the lampreys Petromyzon marinus and Lampetra planeri exhibit conserved molecular asymmetries between the left and right developing habenulae.

Neuronal release and successful astrocyte uptake of aminoacidergic neurotransmitters after spinal cord injury in lampreys.

In contrast to mammals, the spinal cord of lampreys spontaneously recovers from a complete spinal cord injury (SCI). Understanding the differences between lampreys and mammals in their response to SCI could provide valuable information to propose new therapies. Unique properties of the astrocytes of lampreys probably contribute to the success of spinal cord regeneration.

Traumatic injury induces changes in the expression of the serotonin 1A receptor in the spinal cord of lampreys.

After spinal cord injury (SCI) in mammals, the loss of serotonin coming from the brainstem reduces the excitability of motor neurons and leads to a compensatory overexpression of serotonin receptors. Despite the key role of the serotonin receptor 1a in the control of locomotion, little attention has been put in the study of this receptor after SCI. In contrast to mammals, lampreys recover locomotion after a complete SCI, so, studies in this specie could help to understand events that lead to recovery of function.

Aspartate-containing neurons of the brainstem and rostral spinal cord of the sea lamprey Petromyzon marinus: distribution and comparison with γ-aminobutyric acid.

The amino acid L-aspartate (ASP) is one of the most abundant excitatory neurotransmitters in the mammalian brain, but its distribution in other vertebrates has not yet been well characterized. We investigated the distribution of ASP in the brainstem and rostral spinal cord of the adult sea lamprey by using ASP immunohistochemistry. Our results indicate that ASP is accumulated in specific neurons, but not in glia (tanycytes).

Detection methods for microRNAs in clinic practice.

MicroRNAs (miRNA) are short non-coding RNA molecules that regulate gene expression. miRNAs profiles are specific for cell lineages and tissues, and their changes reflect pathological processes. This fact introduces the possibility of their use in diagnostics.

The glutamatergic neurons in the spinal cord of the sea lamprey: an in situ hybridization and immunohistochemical study.

Glutamate is the main excitatory neurotransmitter involved in spinal cord circuits in vertebrates, but in most groups the distribution of glutamatergic spinal neurons is still unknown. Lampreys have been extensively used as a model to investigate the neuronal circuits underlying locomotion. Glutamatergic circuits have been characterized on the basis of the excitatory responses elicited in postsynaptic neurons.