GABA-immunoreactive internuclear neurons in the ocular motor system of lampreys

doi:10.1016/S0006-8993(99)02402-6

Brain Research

Volume 855, Issue 1, 7 February 2000, Pages 150-157

https://doi.org/10.1016/S0006-8993(99)02402-6 Get rights and content

Abstract

The presence of internuclear neurons in the abducens and oculomotor nuclei of lampreys [González, M.J., Pombal, M.A., Rodicio, M.C. and Anadón, R., Internuclear neurons of the ocular motor system of the larval sea lamprey, J. Comp. Neurol. 401 (1998) 1–15] indicates that coordination of eye movements by internuclear neurons appeared early during the evolution of vertebrates. In order to investigate the possible involvement of inhibitory neurotransmitters in internuclear circuits, the distribution of γ-aminobutyric acid (GABA) in the extraocular motor nuclei of the lamprey was studied using immunocytochemical techniques. Small GABA-immunoreactive (GABAir) neurons were observed in the three ocular motor nuclei. Numerous GABAir neurons were observed in the group of internuclear neurons of the dorsal rectus oculomotor subnucleus. A second group of GABAir neurons was observed among and below the trochlear motoneurons. Two further groups of GABAir interneurons, periventricular and lateral, were located in the abducens nucleus among the cells of the caudal rectus and the ventral rectus motor subnuclei, respectively. In addition to the presence of GABAir neurons, in all the ocular motor nuclei the motoneurons were contacted by numerous GABAir boutons. Taken together, these results suggest that GABA is involved as a neurotransmitter in internuclear pathways of the ocular motor system of lampreys.

Introduction

The internuclear neurons of the ocular motor system are neurons located within and around the ocular motor nuclei that project to other oculomotor or oculomotor-related nuclei [13]. These neurons have been observed in mammals since the early 1970s, the abducens internuclear neurons being the best characterized both anatomically and physiologically 1, 16, 19, 33. These cells discharge with patterns similar to those of abducens motoneurons 7, 10, 11, 26 and form excitatory contacts on oculomotor neurons of the medial rectus muscle [18]. The presence of oculomotor internuclear neurons in mammals has also been reported 6, 23, 24, 25, 37, but their connections and role in ocular coordination are poorly understood. A proportion of the oculomotor interneurons in mammals are γ-aminobutyric acid-immunoreactive (GABAir) [8]. GABAir boutons are abundant on the oculomotor and abducens motoneurons of mammals [8]. The presence of abducens internuclear neurons has also been reported in non-mammalian vertebrates: birds 3, 20, 21, reptiles 5, 35, amphibians [34], and teleosts 4, 36. In these vertebrates, the pattern of internuclear connections is again poorly understood. To our knowledge, nothing is known about the presence of GABAergic circuits in the ocular motor system in these groups.

Lamprey eyes have six extraocular muscles that are innervated by the oculomotor nucleus (dorsal rectus, medial rectus, rostral oblique), the trochlear nucleus (caudal oblique), and the abducens nucleus (lateral rectus, ventral rectus) [15]. The topography of ocular motoneuron subnuclei has been described elsewhere in both adult [15] and larval [27] lampreys. In addition to motoneurons, we have also characterized in lampreys two groups of abducens internuclear neurons (lateral and periventricular) and a group of oculomotor internuclear neurons (located in the region of the dorsal rectus subnucleus) using tract-tracing methods [17]. These groups of internuclear neurons appear to have specific connections with some extraocular muscle subnuclei. The aim of the present study was to investigate the presence of GABA in both interneurons and synaptic terminals on the ocular motoneurons in lampreys, in order to elucidate whether this neurotransmitter is involved in the modulation of the ocular motor system.

Section snippets

Animals

Larval and adult lampreys were used in this study. Adult lampreys were of two different species, the sea lamprey (Petromyzon marinus L.: n=4) and the river lamprey (Lampetra fluviatilis L.: n=4). Larval lampreys were of P. marinus, (n=6). Sea lampreys were caught at the Ximonde Biological Station (River Ulla, northwest Spain). River lampreys were caught in Söderhamn (Sweden). Larval lampreys were kept in well-aerated aquariums with a bed of sediment from the river, while adult individuals were

Results

GABAir internuclear neurons were observed in the three ocular motor nuclei in both the sea and river lampreys. In addition, ocular motor neurons received abundant GABAir innervation, both on their perikarya and on dendrites. The location of these GABAir internuclear neurons in the ocular motor nuclei of adult lamprey is summarized in Fig. 1. In larval sea lampreys, the distribution of GABAir ocular motor internuclear neurons was similar to that in the adult, and GABAergic fibers were also

GABA immunoreactivity in the ocular motor nuclei and the life cycle

The present results demonstrate for the first time the presence of four groups of GABAir interneurons that are closely associated with the ocular motor system of lampreys, and reveal abundant GABAir boutons contacting motoneurons in the three nuclei of this system. These findings indicate that this inhibitory neurotransmitter is extensively used in the ocular motor system of lampreys, as in mammals 8, 32. The similar distribution of GABA observed in the ocular motor system of adult and larval

Acknowledgements

The authors wish to thank the Consellerı́a de Medio Ambiente (Dirección Xeral de Montes e Medio Ambiente Natural) of the Xunta de Galicia, for their permission in capturing the sea lampreys used in this study. This work was supported by grants from the Xunta de Galicia (XUGA 20012B96; XUGA 20002B97), the Spanish Education Ministry (PB96-0945-C02), and a predoctoral fellowship (University of Santiago de Compostela) to M.M.-F.

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Although the sample number is small in this study, it suggests that the human trochlear nucleus can be divided into three parts, and that the overall growth may be accelerated at about 30 weeks of gestation.
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Evolution of the deuterostome central nervous system: An intercalation of developmental patterning processes with cellular specification processes
2007, Evolution of Nervous Systems
The morphological, histological, and molecular basis of deuterostome and craniate nervous system organization is reviewed in the context of cladistic evidence of relationships and basic principles of neuroanatomical comparisons. The central nervous system (CNS) of deuterostomes shows a variety of forms, from a hardly specialized basiepithelial nerve plexus (hemichordates), to a few small ganglia with a tail nerve cord (urochordates; or a tailless head in adult sessile urochordates), to a swimming spinal cord with a hardly recognizable cerebral vesicle (cephalochordates), to a fully developed brain and spinal cord (craniates). Despite these overall differences, similarities related to a certain degree of rostrocaudal and dorsoventral patterning are present. These may be directly related to the overall rostrocaudal patterning of the body and to the fact that the neural tube evolved only once in ancestral chordates and has maintained a molecularly identical dorsoventral patterning scheme. This evidence implies that deep homology or homocracy exists among deuterostome (CNS) but that distinct evolutionary adaptations exist that render morphological comparisons of nervous tissue organization among deuterostomes difficult. For example, comparisons at a cellular level show that the motoneurons of deuterostomes share certain basic similarities across taxa but also exhibit unique taxon-specific features that do not appear to follow a progressive evolutionary transformation but rather indicate independently derived transformations from a potentially common root in the basiepithelial nerve plexus of primitive deuterostome taxa. Likewise, comparative analysis of common neuronal cell types identifiable by their specific neurotransmitters demonstrates a variety of patterns of topology and homology. Enough similarities exist to suggest that most of the apparent differences probably represent variations on a theme that may already have been set up in the last common ancestor of all deuterostomes. Moving on to the molecular specification of the cellular topology of the nervous system, the available data provide a promising beginning toward a phylogenetic synthesis but also indicate that the comparison of gene expression domains does not provide a magic bullet to pinpoint basic neuromeric homologies. Evolutionary modifications of gene expression patterns and of patterns of neuronal differentiation within given neuromeres make the road ahead as difficult as the road was until here. Still, the emerging framework of nested gene expression patterns, combined with more sophisticated neuronal tracing studies, will clearly facilitate tracing the origins of region-specific neuronal phenotypes and relating this to specific gene expression domains through gain-of-function and loss-of-function analyses.
The extraocular motor nuclei: Organization and functional neuroanatomy
2006, Progress in Brain Research
Citation Excerpt :
Several populations of internuclear neurons with diverse projection targets, such as the spinal cord, the cerebellum, the abducens nucleus have been identified within and around the oculomotor nucleus (Phipps et al., 1983; Maciewicz et al., 1984; Chung et al., 1987; Clendaniel and Mays, 1994). In lampreys, there is evidence for GABA-immunoreactive neurons within the extraocular motor nuclei (Melendez-Ferro et al., 2000). The best investigated of these interneurons are the oculomotor internuclear neurons (OMN-INT) lying within within the III and in the supraoculomotor area, which project bilaterally to the abducens nucleus.
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Research reportGABA-immunoreactive internuclear neurons in the ocular motor system of lampreys

Abstract

Introduction

Section snippets

Animals

Results

GABA immunoreactivity in the ocular motor nuclei and the life cycle

Acknowledgements

Neuroscience

Neuroscience

Neuroscience

Brain Res.

Exp. Neurol.

Brain Res.

Prog. Brain Res.

Brain Res.

Physiological identification of interneurons and motoneurons in the abducens nucleus

Brain Res.

The biology of the anadromous sea lamprey (Petromyzon marinus)

N. B. J. Zool.

Cytoarchitectonic organisation of the abducens nucleus in the pigeon (Columba livia)

J. Anat.

A morphological study of abducens nucleus motoneurons and internuclear neurons in the goldfish (Carassius auratus)

Brain Res. Bull.

A morphological study of the principal and accessory abducens nuclei in the Caspian terrapin (Mauremys caspica)

Brain Behav. Evol.

Characteristics of antidromically identified oculomotor internuclear neurons during vergence and versional eye movements

J. Neurophysiol.

Behavior of medial rectus motoneurons in the alert cat

Eur. J. Neurosci.

The development of retina and the optic tectum of Petromyzon marinus L. A light microscopic study

J. Hirnforsch.

Research report
GABA-immunoreactive internuclear neurons in the ocular motor system of lampreys