Response of the optic tectum to stimulation of the optic nerve in the teleost Eugerres plumieri

doi:10.1016/0006-8993(71)90636-6

Brain Research

Volume 31, Issue 1, 6 August 1971, Pages 107-118

https://doi.org/10.1016/0006-8993(71)90636-6 Get rights and content

Summary

In the teleost E. plumieri, recordings from the optic tectum in response to electrical stimuli applied to the contralateral optic nerve show 3 small negative peaks (waves 1, 2 and 3) followed by a large negative deflection formed by two components (waves 4 and 5). There follows a positive deflection (wave 6). Waves 1, 2 and 3 are characterized as presynaptic since they: (a) corresponse in latency with 3 fiber groups found in the optic nerve with conduction velocities of approximately 20, 10 and 5 m/sec; (b) retain their polarity throughout the tectal thickness; and (c) coincide in time with unitary spikes which behave as presynaptic elements and are found only in tectal layers that contain nerve fibers. Waves 4, 5 and 6, on the other hand, are characterized as postsynaptic in nature since they: (a) show polarity reversal in electrode penetrations perpendicular to the tectal surface; (b) have excitability cycles typical of postsynaptic responses; and (c) coincide in time with unitary spikes which behave as postsynaptic elements and are found in all tectal layers. Waves 4 and 5 are probably due to postynaptic excitation, and wave 6 is possibly associated with postsynaptic analysis suggest propagated dendritic activity.

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Cited by (31)

Pharmacologic evidence for NMDA, APB and kainate/quisqualate retinotectal transmission in the isolated whole tectum of goldfish
1990, Brain Research
The optic tectum of goldfish with intact optic and toral marginal fiber tracts was isolated in a perfusion chamber where the effectiveness of antagonists was tested on synaptic field potential responses to stimulation of each afferent system. There were 3 main conclusions about excitatory synapses. First, monosynaptic activation of retinotectal synapses was not detectably antagonized byd-tubocurarine, implying there is no nicotinic cholinergic component to optic transmission nor strong cholinergic gating of optic terminals. Second, a significant component of retinotectical transmission was shown to be mediated by kainate and quisqualate receptors since 6,7-dinitroquinoxaline-2,3-dione and kynurenate strongly suppressed the optic field potential. In addition, activation of these synapses involves two previously undescribedN-methyl-d-aspartate (NMDA) and APB receptor subtypes since optic field potentials were partially suppressed by 2-amino-5-phosphonovalerate (APV), 2-amino-4-phosphonobutyrate (APB) and MK-801. This is the first evidence that APB receptors exist in the visual system central to the retina. Together, these results are consistent with the possibility that retinal ganglion cells use multiple glutamate receptor subtypes. Third, the optic tectum contains a population of intrinsic glutaminergic synapses activated by a non-optic input, the marginal fibers, which can be suppressed by both APV and kynurenate. The existence of tectal NMDA receptors whicha are not at primary optic synapses implies that APV used to interfere with rearrangement of optic fibers during development may act not only at afferent synapses but also at a more central component of the circuit.
Long-term potentiation in the goldfish optic tectum
1986, Brain Research
Field potential recordings were made in the primary retinal synaptic area, the stratum fibrosum et griseum superficiale (SFGS), of an in vitro goldfish optic tectum preparation. Stimulation of the optic nerve at frequencies of 1 and 5 Hz produced a long-term potentiation (LTP) of the synaptic response which developed gradually. No potentiation was seen with lower or higher frequencies. These results demonstrate a significant LTP with a slow time course and restricted low-frequency dependence.
Sensory representation in the cerebellum of the catfish
1984, Neuroscience
Sensory representation in the catfish cerebellum was studied with physiological stimuli, with electric shocks applied to peripheral nerves and with electric shocks to central structures of the brain. Evoked field potentials and unit responses were recorded in different places in the cerebellum. In the catfish, different sensory modalities are represented by discrete, only partly overlapping areas of the cerebellum. Most units are unimodal by present criteria; only in the valvula a fraction of the units are responsive to two or more modalities. Visual and somatosensory areas are the largest and they occupy the bulk of the corpus cerebelli and the valvula. In the corpus, most of the visual units are near the midline and in the dorsal tier while the somatosensory units are more lateral and ventral. Mechanical lateral line input is represented in the eminentia granularis and the valvula. Acoustic units are found in the valvula. Electroreceptive units are recorded from the lateral lobus caudalis, and to a lesser degree, from the eminentia granularis and valvula. Sinusoidal tilting and vibration units are in the lobus caudalis pars medialis. Receptive fields of units, regardless of modality, are generally large and diffuse. Some visual units respond best to moving objects. Topographical organization of receptive fields only exists among the somatosensory units.
Besides these findings of modality segregation, the features of interest for comparative neurology are the following. Most units are identifiable as Purkinje cells with a characteristic mossy fiber-granular cell pattern, and but in contrast to most experience with mammals, in response to direct brain or nerve stimulations, the simple spikes have different dynamic responses for different modalities. Some are first excited, then inhibited, others vice versa. Some units are not responsive to any sensory input we delivered. Some units not meeting the criteria for Purkinje cells meet several criteria for eurydendroid cells; they give large spikes and are influenced by sensory stimuli after relative long latencies. Complex spikes, however, were only consistently observed in some of the visual units.
Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum
1983, Brain Research Reviews
The present paper is aimed at an exploration of the possible functional significance of the laminar organization of the goldfish tectum at both the cellular and the synaptic level. For this purpose
- 1.
  (1) the data concerning the structure of the teleostean tectum are surveyed,
- 2.
  (2) a conceptual framework of the intratectal connectivity in the goldfish is proposed,
- 3.
  (3) the electrophysiological data concerning the teleostean tectum are surveyed and
- 4.
  (4) the degree of correlation between the structural and physiological data available is discussed.
Apart from the retina, tectal afferents originate from at least 10 other brain centers. At least 5 of these projections appear to be topographically organized. Tectal afferents, neurons as well as synapses reveal a characteristic intratectal lamination pattern. Tectal efferents project to at least 10 brain centers, and have until now been shown to arise from 6 cell types.
The structural data surveyed allow the construction of a conceptual framework of tectal circuitry on the basis of 3 starting points.
- 1.
  (1) The existence of at least 8 presynaptic zones or laminae, each containing a characteristic set of presynaptic structures (afferents and axons of interneurons).
- 2.
  (2) The fact that the tectal postsynaptic structures (somata and dendrites of tectal neurons) each have a characteristic location, extension and synaptic density, which determines the relative importance of the different presynaptic zones for each cell type.
- 3.
  (3) The laminar specificity hypothesis, which implies that presynaptic structures that coexist in a particular presynaptic zone terminate without preference on all types of postsynaptic structures within that zone.
The conceptual framework of tectal circuitry is quantified in terms of connectivity index and connective importance.
Analysis of the framework constructed leads to a detailed description of the intratectal pathways involved in the processing of the 4 main streams of tectal input (i.e. visual, toral, telencephalic and ‘deep’ input). It was concluded that the laminar organization of the tectum is primarily relevant for multimodal integration and that the tectal cell types each receive a characteristic sample out of the multimodal information available in the different tectal layers.
The physiological data available do not yet allow testing of the tentative conclusion formulated for two main reasons:
- 1.
  (1) the tectal units which have been electrophysiologically investigated have only rarely been identified morphologically; and
- 2.
  (2) by far most physiological studies exclusively used visual stimulation or electrical stimulation of the optic nerve, whereas other modalities or tectal afferents have only incidentally received physiological attention.
The combined topographical and laminar organization of the teleostean tectum is in particular suitable for the localization and selection of objects in the environment on the basis of integrated multimodal information (including visual, acoustical, lateral line and tactile information) and the subsequent orientation of the eyes, head and/or body toward or away from selected objects. This general tectal function appears to be constant throughout all classes of vertebrates¹⁰². However, the underlying intratectal mechanisms are far from understood. It is hoped that the present paper provides a functional anatomical framework which facilitates a further elucidation of these mechanisms in the tectum of teleosts.
Morphological aspects of the teleostean visual system: A review
1983, Brain Research Reviews
This review is concerned with results of research carried out in the last two decades regarding visual pathways and centers in teleosts. It covers neither morphology of the retina nor development and plasticity. The optic nerve is considered in terms of axonal composition and retinotopic organization. The connections to the retina and from the retina are subsequently reviewed, and a general scheme is proposed for the retinofugal targets in thalamus and pretectum. The tectum opticum is then reviewed as regards its afferent connections from retina, telencephalon, diencephalon, mesencephalon and brainstem, with details on distribution of terminals, cell types contacted and synaptic structure. The efferent tectal connections are reviewed next, including their plausible cells of origin. Finally, a general diagram of the teleostean visual system is presented, and several circuits within this diagram are emphasized and discussed.
An intracellular study of the optic tectum of the carp in vitro
1983, Neuroscience Letters
Intracellular recordings were performed on the optic tectum of the carp in vitro. Thick brain sections were prepared and the optic tract was electrically stimulated. EPSPs of 72 cells in stratum fibrosum et griseum superficiale, stratum griseum centrale and stratum album centrale were examined. Monosynaptic EPSPs were recorded from 19 cells in stratum fibrosum et griseum centrale and stratum griseum centrale, which was consistent with anatomical findings.

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Brain Research

Summary

References (27)

Relation between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and epicortical stimulation

Electroenceph. clin. Neurophysiol.

Interpretation of action potentials evoked in the cerebral cortex

Electroenceph. clin. Neurophysiol.

The electric response evoked in the reptilian optic tectum by afferent stimulation

Brain Research

Spectral analysis of L-type S-potentials and their relation to photopigment absorption in a fish (Eugeres plumieri) retina

Vision Res.

Lateral spread of light-induced potentials along different cell layers in the teleost retina

Vision Res.

Der visuelle Greifreflex

Helv. physiol. pharmacol. Acta

Problems and methods of anatomical localization

Interhippocampal impulses. II. Apical dendritic activation of CA₁ neurons

Acta physiol. scand.

Fiber groups in the optic nerve

Amer. J. Physiol.

Analyse des RésponsesÉlectriques du Lobe Optiqueàla Stimulation de la Voie Visuelle chez Quelques Vertébrés Inférieurs

The optic tectum of Gallus domesticus: a correlation of the electrical responses with histological structure

J. Anat. (Lond.)

The Physiology of Nerve Cells

Cited by (31)

Pharmacologic evidence for NMDA, APB and kainate/quisqualate retinotectal transmission in the isolated whole tectum of goldfish

Long-term potentiation in the goldfish optic tectum

Sensory representation in the cerebellum of the catfish

Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum

Morphological aspects of the teleostean visual system: A review

An intracellular study of the optic tectum of the carp in vitro

Response of the optic tectum to stimulation of the optic nerve in the teleost Eugerres plumieri

Summary

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Brain Research

Vision Res.

Vision Res.

Der visuelle Greifreflex

Helv. physiol. pharmacol. Acta

Problems and methods of anatomical localization

Interhippocampal impulses. II. Apical dendritic activation of CA1 neurons

Acta physiol. scand.

Fiber groups in the optic nerve

Amer. J. Physiol.

Analyse des RésponsesÉlectriques du Lobe Optiqueàla Stimulation de la Voie Visuelle chez Quelques Vertébrés Inférieurs

The optic tectum of Gallus domesticus: a correlation of the electrical responses with histological structure

J. Anat. (Lond.)

The Physiology of Nerve Cells

Interhippocampal impulses. II. Apical dendritic activation of CA₁ neurons