Retinal projections in larval, transforming and adult sea lamprey, <i>Petromyzon marinus</i>

Kennedy, Michael; Rubinson, Kalman

doi:10.1002/cne.901710404

Cited by 78 publications

(55 citation statements)

References 25 publications

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“…Following application of biocytin in the eye bulb, both retinofugal and retinopetal connections were revealed, as previously reported by using other techniques [Kennedy and Rubinson, 1977;Kosareva, 1980;Repérant et al, 1980Repérant et al, , 1982Vesselkin et al, 1980Vesselkin et al, , 1984Vesselkin et al, , 1996Vesselkin and Repérant, 1985;De Miguel et al, 1990;Rodicio et al, 1995]. Briefly, retinofugal fibers of the optic tract projected mostly to the superficial layers of the contralateral OT (SM and SO) and constituted the lateral and axial optic tracts, whereas the retinopetal cells distributed in the M5 nucleus of Schöber and the mesencephalic reticular area ( fig.…”

Section: Complementary Experimentssupporting

confidence: 70%

“…Retinal projections in larval, transforming, and adult lampreys have been the matter of numerous experimental studies [Northcutt and Przybylski, 1973;Kennedy and Rubinson, 1977;Kosareva et al, 1977;Kosareva, 1980;Repérant et al, 1980;Vesselkin et al, 1980Vesselkin et al, , 1984De Miguel et al, 1990]. Data presented by these authors demonstrated the presence of a major contralateral retinal projection to the OT, but also a small ipsilateral projection.…”

Section: Introductionmentioning

confidence: 99%

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

Arriba

Pombal²

2006

Brain Behav Evol

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Tectal afferents were studied in adult lampreys of three species (Ichthyomyzon unicuspis, Lampetra fluviatilis, and Petromyzon marinus) following unilateral BDA injections into the optic tectum (OT). In the secondary prosencephalon, neurons projecting to the OT were observed in the pallium, the subhipoccampal lobe, the striatum, the preoptic area and the hypothalamus. Following tectal injections, backfilled diencephalic cells were found bilaterally in: prethalamic eminence, ventral geniculate nucleus, periventricular prethalamic nucleus, periventricular pretectal nucleus, precommissural nucleus, magnocellular and parvocellular nuclei of the posterior commissure and pretectal nucleus; and ipsilaterally in: nucleus of Bellonci, periventricular thalamic nucleus, nucleus of the tuberculum posterior, and the subpretectal tegmentum, as well as in the pineal organ. At midbrain levels, retrogradely labeled cells were seen in the ipsilateral torus semicircularis, the contralateral OT, and bilaterally in the mesencephalic reticular formation and inside the limits of the retinopetal nuclei. In the hindbrain, tectal projecting cells were also bilaterally labeled in the dorsal and lateral isthmic nuclei, the octavolateral area, the sensory nucleus of the descending trigeminal tract, the dorsal column nucleus and the reticular formation. The rostral spinal cord also exhibited a few labeled cells. These results demonstrate a complex pattern of connections in the lamprey OT, most of which have been reported in other vertebrates. Hence, the lamprey OT receives a large number of nonvisual afferents from all major brain areas, and so is involved in information processing from different somatic sensory modalities.

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Section: Complementary Experimentssupporting

confidence: 70%

Section: Introductionmentioning

confidence: 99%

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

Arriba

Pombal²

2006

Brain Behav Evol

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“…The visual projections terminate mainly in the superficial layers of the contralateral tectum in lamprey (Kennedy and Rubinson 1977;Rio et al 1996) as in teleosts (for review, see Meek 1983). The organization of the retinotectal projections in the latter have been studied in several species (Schwassman and Kruger 1965) and a retinotopic organization similar to that of the mammalian superior colliculus has been demonstrated.…”

Section: The Input Channels To the Lamprey Tectummentioning

confidence: 99%

“…The optic tectum is a main target of visual inputs from retinal ganglion cells in lower vertebrates such as lamprey (Kennedy and Rubinson 1977;Nieuwenhuys and Nicholson 1998), goldfish (Meyer 1980;Stuermer and Raymond 1989), and zebrafish (Baier et al 1996;Stuermer 1988). The laminated structures of the optic tectum in cyclostomes (Iwahori et al 1996(Iwahori et al , 1999) and teleosts (Meek 1983;Sajovic and Levinthal 1982) are similar to those of the mammalian superior colliculus (Warton and Jones 1985).…”

Section: Introductionmentioning

confidence: 99%

Tectal Control of Locomotion, Steering, and Eye Movements in Lamprey

Saitoh

Ménard

Grillner

2007

Journal of Neurophysiology

101

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Saitoh K, Ménard A, Grillner S. Tectal control of locomotion, steering, and eye movements in lamprey. J Neurophysiol 97: 3093-3108, 2007. First published February 15, 2007 doi:10.1152/jn.00639.2006. The intrinsic function of the brain stem-spinal cord networks eliciting the locomotor synergy is well described in the lamprey-a vertebrate model system. This study addresses the role of tectum in integrating eye, body orientation, and locomotor movements as in steering and goal-directed behavior. Electrical stimuli were applied to different areas within the optic tectum in head-restrained semi-intact lampreys (n ϭ 40). Motions of the eyes and body were recorded simultaneously (videotaped). Brief pulse trains (Ͻ0.5 s) elicited only eye movements, but with longer stimuli (Ͼ0.5 s) lateral bending movements of the body (orientation movements) were added, and with even longer stimuli locomotor movements were initiated. Depending on the tectal area stimulated, four characteristic response patterns were observed. In a lateral area conjugate horizontal eye movements combined with lateral bending movements of the body and locomotor movements were elicited, depending on stimulus duration. The amplitude of the eye movement and bending movements was site specific within this region. In a rostromedial area, bilateral downward vertical eye movements occurred. In a caudomedial tectal area, largeamplitude undulatory body movements akin to struggling behavior were elicited, combined with large-amplitude eye movements that were antiphasic to the body movements. The alternating eye movements were not dependent on vestibuloocular reflexes. Finally, in a caudolateral area locomotor movements without eye or bending movements could be elicited. These results show that tectum can provide integrated motor responses of eye, body orientation, and locomotion of the type that would be required in goal-directed locomotion.

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“…Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23)(24)(25)(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).…”

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confidence: 99%

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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Retinal projections in larval, transforming and adult sea lamprey, Petromyzon marinus

Cited by 78 publications

References 25 publications

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

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

Tectal Control of Locomotion, Steering, and Eye Movements in Lamprey

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

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