Afferent Connections of the Optic Tectum in Lampreys: An Experimental Study

Arriba, María del Carmen de; Pombal, Manuel A.

doi:10.1159/000095272

Cited by 57 publications

(33 citation statements)

References 372 publications

(336 reference statements)

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“…Afferents from cortex (pallium in nonmammals) thus provide monosynaptic excitation to tectal output cells in lamprey (Fig. 8D) as in other species (54)(55)(56). Furthermore, the basal ganglia output nuclei instead provide tonic GABAergic inhibition to the tectal output cells in lamprey as well as in mammals (31,(57)(58)(59).…”

Section: Discussionmentioning

confidence: 98%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

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

132

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The optic tectum (called superior colliculus in mammals) is critical for eye-head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex-yet phylogenetically conservedsensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gazecontrolling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.optic tectum | superior colliculus | GABAergic inhibition | gaze control | evolution V isual scenes are composed of abundant stimuli, and the gaze needs continuously to be redirected toward different objectsan important task for the brain. Current models postulate that stimulus selection occurs through a process involving competitive interaction between different visual stimuli, resulting in the appropriate eye-head movement (1-5). The optic tectum (superior colliculus in mammals) has a causal role in the stimulus selection process (6-12) and not only in the control of saccades and eyehead gaze shifts (13-16). Although the collicular contribution to the selection process is of central importance, the underlying neuronal processes have remained elusive due to methodological limitations. It is our aim here to address this issue in a novel experimental model.The optic tectum is well developed in the lamprey, belonging to the oldest extant vertebrate group that evolved 560 million years ago (17), and it has remained conserved throughout vertebrate phylogeny (18)(19)(20)(21)(22). Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23-26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).To uncover the mechanisms underlying visual stimulus selection for gaz...

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Section: Discussionmentioning

confidence: 98%

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Kardamakis

Saitoh

Grillner

2015

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

132

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“…The torus semicircularis of the lamprey receives a large number of fibers from vestibular and lateral line centers (Gonzá lez et al, 1999) and is comparable to the inferior colliculus of mammals, whereas the optic tectum is the main visual center and is homologous to the superior colliculus (De Arriba Pérez, 2007;De Arriba and Pombal, 2007). However, in situ hybridization did not reveal GlyT-2 transporter mRNA in cells in the inferior colliculus of either rats or mice (Tanaka and Ezure, 2004;Zeilhofer et al, 2005), whereas occasional glycinergic cells appeared in the superior colliculus (Zeilhofer et al, 2005).…”

Section: The Midbrain Glycine-ir Cell Populations Of the Lamprey Are mentioning

confidence: 99%

“…Several nuclei of the isthmic region project to the optic tectum (Robertson et al, 2006;De Arriba and Pombal, 2007), and this region also has a number of glycine-ir populations, some of which may project to the tectum. Although only occasional putative glycinergic cells have been observed in the superior colliculus of mammals (Tanaka and Ezure, 2004), glycinergic fibers appear rather abundant (Rampon et al, 1996).…”

Section: The Midbrain Glycine-ir Cell Populations Of the Lamprey Are mentioning

confidence: 99%

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

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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.

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“…The chapter contains an extensive list of the localisation of neurotransmitters and other neuronal substances in the lamprey brain. More recent data on brain neurochemical distribution, proliferation and connectivity, or data not mentioned in this list, include the work of (Abalo et al 2005;Auclair et al 2004;de Arriba Mdel and Pombal 2007;de Miguel et al 1990;Del Carmen De Andres et al 2002;Frontini et al 2003;Gonzalez et al 1999;Laframboise et al 2007;Melendez-Ferro et al 2002a, 2002bMenard et al 2007;Osorio et al 2006;PerezCostas et al 2002PerezCostas et al , 2004Pflieger and Dubuc 2004;PierreSimons et al 2002;Pombal et al 1997aPombal et al , 1997bPombal et al , 2001Robertson et al 2006Robertson et al , 2007Root et al 2005;Vidal Pizarro et al 2004;Villar-Cheda et al 2002, 2006Weigle and Northcutt 1999). Neuronal phenotype distribution and fibre connectivity in the lamprey brain have also been reviewed by Wullimann and Vernier (2006).…”

Section: The Lamprey Brain: Adult Featuresmentioning

confidence: 99%

The lamprey in evolutionary studies

2008

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Lampreys are a key species to study the evolution of morphological characters at the dawn of Craniates and throughout the evolution of the craniate's phylum. Here, we review a number of research fields where studies on lampreys have recently brought significant and fundamental insights on the timing and mechanisms of evolution, on the amazing diversification of morphology and on the emergence of novelties among Craniates. We report recent example studies on neural crest, muscle and the acquisition of jaws, where important technical advancements in lamprey developmental biology have been made (morpholino injections, protein-soaked bead applications or even the first transgenesis trials). We describe progress in the understanding and knowledge about lamprey anatomy and physiology (skeleton, immune system and buccal secretion), ecology (life cycle, embryology), phylogeny (genome duplications, monophyly of cyclostomes), paleontology, embryonic development and the beginnings of lamprey genomics. Finally, in a special focus on the nervous system, we describe how changes in signaling, neurogenesis or neuronal migration patterns during brain development may be at the origin of some important differences observed between lamprey and gnathostome brains.

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Afferent Connections of the Optic Tectum in Lampreys: An Experimental Study

Cited by 57 publications

References 372 publications

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

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

The lamprey in evolutionary studies

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