GABA distribution in lamprey is phylogenetically conserved

Robertson, Brita; Auclair, François; Ménard, Ariane; Grillner, Sten; Dubuc, Réjean

doi:10.1002/cne.21348

Cited by 73 publications

(128 citation statements)

References 116 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The respiratory responses obtained following blockade of GABAergic and glycinergic neurotransmission within these regions are corroborated by the results on GABA and glycine immunoreactivity. Present findings on GABA and glycine immunoreactivity within the respiratory motor column of the lamprey are in agreement with previous results (Robertson et al, 2007;Villar-Cervin˜o et al, 2008). In this study, evidence has been provided that retrogradely labeled neurons are surrounded by GABA immunoreactivity and that GABAimmunoreactive structures are in close apposition to these cells, suggesting the presence of synaptic terminals.…”

Section: Discussionsupporting

confidence: 93%

“…In addition, the fact that microinjections of glutamate antagonists or muscimol were ineffective implies that, like the respiratory motor region, the OLA is also not involved in respiratory rhythm generation, but can increase the respiratory frequency when its neurons are brought into action by disinhibition or activation. Our immunohistochemical results concerning the OLA are consistent with previous results (Robertson et al, 2007;Villar-Cervin˜o et al, 2008. It can also be mentioned that not only ascending projections from the respiratory motor column, but also those from the OLA could obviously contribute to the respiratory responses obtained by bath application of bicuculline or strychnine (Bongianni et al, 2006).…”

Section: Ascending Excitatory Projections From the Ola To The Ptrgsupporting

confidence: 92%

“…Although the rabbit anti-GABA antibody has not been previously used in the lamprey, we are confident that it is specific for GABA. In fact, the pattern of distribution of labeled cells that this antibody produces is similar to that obtained with different anti-GABA antibodies (Robertson et al, 2007;Villar-Cervin˜o et al, 2008;Cinelli et al, 2014).…”

Section: Anatomical Experimentssupporting

confidence: 72%

“…The localization of labeled cells was reported on schematic drawings of individual transverse sections. The nomenclature used for anatomical structures is the same as in previous studies (Robertson et al, 2007;Villar-Cervin˜o et al, 2008;Cinelli et al, 2013Cinelli et al, , 2014. The number of neurons in the ipsi-and contralateral side of each investigated area was compared using unpaired t-tests (GraphPad Prism 5, La Jolla, CA, USA).…”

Section: Anatomical Experimentsmentioning

confidence: 99%

See 3 more Smart Citations

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

et al. 2016

View full text Add to dashboard Cite

Abstract-Neurons within the vagal motoneuron region of the lamprey have been shown to modulate respiratory activity via ascending excitatory projections to the paratrigeminal respiratory group (pTRG), the proposed respiratory rhythm generator. The present study was performed on in vitro brainstem preparations of the lamprey to provide a characterization of ascending projections within the whole respiratory motoneuron column with regard to the distribution of neurons projecting to the pTRG and related neurochemical markers. Injections of Neurobiotin were performed into the pTRG and the presence of glutamate, GABA and glycine immunoreactivity was investigated by doublelabeling experiments. Interestingly, retrogradely labeled neurons were found not only in the vagal region, but also in the facial and glossopharyngeal motoneuron regions. They were also present within the sensory octavolateral area (OLA). The results show for the first time that neurons projecting to the pTRG are immunoreactive for glutamate, surrounded by GABA-immunoreactive structures and associated with the presence of glycinergic cells. Consistently, GABA A or glycine receptor blockade within the investigated regions increased the respiratory frequency. Furthermore, microinjections of agonists and antagonists of ionotropic glutamate receptors and of the GABA A receptor agonist muscimol showed that OLA neurons do not contribute to respiratory rhythm generation. The results provide evidence that glutamatergic ascending pathways to the pTRG are subject to a potent inhibitory control and suggest that disinhibition is one important mechanism subserving their function. The general characteristics of inhibitory control involved in rhythmic activities, such as respiration, appear to be highly conserved throughout vertebrate evolution.

show abstract

Section: Discussionsupporting

confidence: 93%

Section: Ascending Excitatory Projections From the Ola To The Ptrgsupporting

confidence: 92%

Section: Anatomical Experimentssupporting

confidence: 72%

Section: Anatomical Experimentsmentioning

confidence: 99%

See 2 more Smart Citations

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

et al. 2016

View full text Add to dashboard Cite

show abstract

“…4). The two different locomotor command regions both receive tonic input from the inhibitory output neurons of the pallidum-an evolutionarily conserved organization found from lamprey to mammals (43). By including a population of pallidal neurons in the simulations, it has been possible to elicit CPG activity through a release from pallidal inhibition of a reticulospinal population involved in the control of locomotion.…”

Section: Discussionmentioning

confidence: 99%

Simple cellular and network control principles govern complex patterns of motor behavior

Kozlov

Huss²,

Lansner³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

The vertebrate central nervous system is organized in modules that independently execute sophisticated tasks. Such modules are flexibly controlled and operate with a considerable degree of autonomy. One example is locomotion generated by spinal central pattern generator networks (CPGs) that shape the detailed motor output. The level of activity is controlled from brainstem locomotor command centers, which in turn, are under the control of the basal ganglia. By using a biophysically detailed, full-scale computational model of the lamprey CPG (10,000 neurons) and its brainstem/forebrain control, we demonstrate general control principles that can adapt the network to different demands. Forward or backward locomotion and steering can be flexibly controlled by local synaptic effects limited to only the very rostral part of the network. Variability in response properties within each neuronal population is an essential feature and assures a constant phase delay along the cord for different locomotor speeds.basal ganglia ͉ brainstem ͉ computational model ͉ lamprey ͉ spinal CPG V ertebrate behavior depends on different sets of neuronal networks specialized to coordinate different motor tasks like locomotion, breathing, and the expression of emotions (1-5). The activity of these networks is governed by brainstem command centers that are, in turn, under the control of the basal ganglia (1, 2). Although the critical role of these networks is well established, their intrinsic mode of operation has, for the most part, remained enigmatic. The lamprey nervous system provides one of the few examples in which detailed knowledge is available, not only of the different types of the participating neurons, but also their membrane properties and synaptic connectivity, particularly with regard to the spinal network (6, 7). Even with this knowledge at hand, it is very difficult, if not impossible, to establish, without the help of modeling, whether the experimental data available are actually sufficient to account for the dynamic operation of the networkand enable exploration of the particular role of different cellular and synaptic components to make predictions of their functional role. To achieve this, we report here a biophysically realistic model of the locomotor network and its control from the brain. The spinal network is composed of excitatory and inhibitory model neurons that, in considerable detail, behave as their biological counterparts. It proved to be important to introduce within each pool of model neurons the known biological variability in neuronal size and membrane properties. Thanks to recent developments in computer technology, we have been able to make a full-scale model of the network with 100 model neurons per segment, each of the Hodgkin-Huxley type-altogether 10,000 neurons connected via 760,000 synapses in the 100 segments. We represent the brainstem command system, as well as the forebrain control from the basal ganglia with an additional 3,500 neurons. Simulations limited to subsamples of neurons have previou...

show abstract

Distribution of glycine immunoreactivity in the brain of adult sea lamprey (Petromyzon marinus). Comparison with γ‐aminobutyric acid

Villar-Cerviño

Barreiro‐Iglesias

Anadón

et al. 2008

J of Comparative Neurology

View full text Add to dashboard Cite

The distribution of glycinergic cells in the brain of nonmammalian vertebrates is still unknown. Lampreys are the most primitive extant vertebrates, and they may provide important data on the phylogeny of this system. Here, we studied for the first time the distribution of glycine immunoreactivity in the sea lamprey brain and compared it with gamma-aminobutyric acid (GABA)-ergic populations. Most glycine-immunoreactive neurons were found at midbrain and hindbrain levels, and most of these cells did not exhibit GABA immunoreactivity. We describe glycine-immunoreactive cell populations in the olfactory bulbs, the preoptic nucleus, and the thalamus of the sea lamprey, which is in striking contrast to their lack in the mammalian forebrain. We also observed glycine-immunoreactive populations in the optic tectum, the torus semicircularis and the midbrain tegmentum, the isthmus, the octavolateral area, the dorsal column nucleus, the abducens nucleus, the trigeminal motor nucleus, the facial motor nucleus, and the rhombencephalic reticular formation. In these populations, colocalization with GABA was observed in only some cells of the tegmental M5 nucleus, ventral isthmus, medial octavolateral nucleus, dorsal column nucleus, and lateral reticular region. The present results allow us to conclude that the distribution of glycine-immunoreactive cells changed notably from lamprey to mammals, with a decrease in glycinergic populations in the forebrain and a specialization of brainstem cell groups. Although knowledge of the glycinergic populations in lampreys is important for understanding the early evolution of this system, there is a notable gap of information regarding its organization in brains of other nonmammalian vertebrates.

show abstract

GABA distribution in lamprey is phylogenetically conserved

Cited by 73 publications

References 116 publications

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

Inhibitory control of ascending glutamatergic projections to the lamprey respiratory rhythm generator

Simple cellular and network control principles govern complex patterns of motor behavior

Distribution of glycine immunoreactivity in the brain of adult sea lamprey (Petromyzon marinus). Comparison with γ‐aminobutyric acid

Contact Info

Product

Resources

About