Reorganization of retinotectal projection following surgical operations on the optic tectum in goldfish

doi:10.1016/0014-4886(71)90031-8

Experimental Neurology

Volume 33, Issue 2, November 1971, Pages 395-411

https://doi.org/10.1016/0014-4886(71)90031-8 Get rights and content

Abstract

The pattern of neural reconnection between the retina and surgically operated tectum was studied in juvenile goldfish (8–11 cm long) with electrophysiological methods. The results confirm that the remaining rostral half-tectum reacquires a complete visual projection from the whole retina about 90 days after excision of the caudal half. The same reorganization of visual projection from the whole retina onto the rostral half-tectum was found to occur in the presence of the caudal half of the tectum, if the two halves were separated by a transverse surgical incision down to the level of the optic ventricle regardless of whether the contralateral optic nerve was left intact or crushed to regenerate. The reorganization of retinotectal projection was also found to occur biaxially along the mediolateral as well as the rostrocaudal axis of the tectum following excision of a caudomedial sector of the tectum. It is suggested that the reorganization of retinotectal projection is due to synaptic respecifications of individual tectal neurons in correct retinotopic order, and that the cellular discontinuity between the rostral and the caudal parts of the tectum is sufficient to induce the orderly synaptic respecifications in juvenile goldfish.

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But several studies challenged Sperry’s chemoaffinity hypothesis (Gaze et al., 1963; Gaze et al., 1965; Meyer, 1998). For instance, in experiments with half retinas, allowing animals to survive for longer periods after surgery resulted in the half retinas innervating the entire tectal lobe, forming a scaled topographic projection (Yoon, 1971; Yoon, 1972). Furthermore, when the caudal half of the tectum was ablated, regenerated axon projections from the entire retina formed a compressed and topographically organized map within the remaining target space.
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A message about the tasks set or solved by a specific nerve center should be transmitted by output neurons to other strictly defined centers of the brain, but not necessarily to certain neurons of the same centers. From this point of view, it is easy to interpret the results of experiments, in which, after the destruction of a half of the visual cortex, the projection of the entire retina, determined by the axons of the glia cells, is compressed in an orderly manner to the size of the entire remaining region of the corpora quadrigemina (Yoon, 1971). As mentioned earlier, MCCs of neurons of a certain type are able to solve a certain set of problems after differentiation.
Efim A. Liberman (1925–2011) can be considered as a founder of the new field of science that explores natural computation and its limits. He named it Chaimatics and suggested its generalization to the ultimate all-encompassing theory that unites biology, physics and mathematics. He made a number of experimental discoveries, including color coding in the retina, the participation mechanisms of Ca²⁺ ions in synaptic transmission, and the measurement of potential in the coupling membranes of mitochondria and chloroplasts. He also made a decisive contribution to the proof of the chemiosmotic hypothesis of oxidative phosphorylation. In a series of works started in 1972, Liberman developed the concept of the molecular computer of the cell, which includes the programs written on DNA and RNA nucleotide sequences and executed by enzymes playing the role of processing units whereas nucleotide sequences are interpreted as commands and addresses. In this framework, Liberman predicted RNA splicing before its discovery and suggested the role of processing of small informational molecules (later defined as small RNAs) in controlling biological processes. Efim Liberman defined the fundamental property of life as a molecular and quantum computational system and introduced the idea of quantum computing inside a cell for making decisions on complex control tasks described by equations of mathematical physics. He approached the brain as a net of molecular computers and created a model of neuron operation based on the transmission of hypersound signals via cytoskeleton where the molecular computational system encodes the digital output. In 1979 Liberman published a hypothesis of human self-consciousness associated with not a chemical, but with a physical quantum coherent system and named it “extremal quantum regulator”. We review here the contributions of Liberman in understanding the mechanisms of intracellular processing of information and his efforts to create an integrative theory of natural computation that aims to unite biology, physics and mathematics.
Chemoaffinity in topographic mapping revisited - Is it more about fiber-fiber than fiber-target interactions?
2014, Seminars in Cell and Developmental Biology
Citation Excerpt :
Double temporal (TT) or double nasal (NN) retinae microsurgically assembled in the larvae, instead of forming doubly occupied maps on their respective tectal halves, matured into expanded projections of each half-retina on the whole target (“compound eye experiments”; [21]). Conversely, tectal ablations (anterior or posterior half) in the goldfish (Fig. 1C), irrespective of concomitant nerve transection, yielded compressed maps of the full retina on the remaining half-target (“compression experiments”; [22–24]). Notably, without nerve transection, this implies mobilization of maturely connected axons of the remaining half-tectum.
Axonal projections between two populations of neurons, which preserve neighborhood relationships, are called topographic. They are ubiquitous in the brain. The development of the retinotectal projection, mapping the retinal output onto the roof of the midbrain, has been studied for decades as a model system. The rigid precision of normal retinotopic mapping has prompted the chemoaffinity hypothesis, positing axonal targeting to be based on fixed biochemical affinities between fibers and targets. In addition, however, abundant evidence has been gathered mainly in the 1970s and 80s that the mapping can adjust to variegated targets with stunning flexibility demonstrating the extraordinary robustness of the guidance process. The identification of ephrins and Eph-receptors as the underlying molecular cues has mostly been interpreted as supporting the fiber–target chemoaffinity hypothesis, while the evidence on mapping robustness has largely been neglected. By having a fresh look on the old data, we expound that they indicate, in addition to fiber–target chemoaffinity, the existence of a second autonomous guidance influence, which we call fiber–fiber chemoaffinity. Classical in vitro observations suggest both influences be composed of opposing monofunctional guidance activities. Based on the molecular evidence, we propose that those might be ephrin/Eph forward and reverse signaling, not only in fiber–target but also in fiber–fiber interactions. In fact, computational models based on this assumption can reconcile the seemingly conflicting findings on rigid and flexible topographic mapping. Supporting the suggested parsimonious and powerful mechanism, they contribute to an understanding of the evolutionary success of robust topographic mass wiring of axons.
Growth dynamics and morphology of regenerating optic fibers in tectum are altered by injury conditions: An in vivo imaging study in goldfish
2008, Experimental Neurology
The dynamic behavior of axons in systems that normally regenerate may provide clues for promoting regeneration in humans. When the optic nerve is severed in adult goldfish, all axons regenerate back to the tectum to reestablish accurate connections. In adult mammals, regeneration can be induced in optic and other axons but typically few fibers regrow and only for short distances. These conditions were mimicked in the adult goldfish by surgically deflecting 10–20% of optic fibers from one tectum into the opposite tectum which was denervated of all other optic fibers by removing its corresponding eye. At 21–63 days, DiI was microinjected into retina to label a few fibers and the fibers were visualized in the living fish for up to 5–7 h. The dynamic behavior and morphology of these regenerating deflected fibers were analyzed and compared to those regenerating following optic nerve crush. At 3–4 weeks, deflected fibers were found to form more branches and to maintain many more branches than crushed fibers. Although both deflected and crushed fibers exhibited stochastic growth and retraction, deflected fibers spent more time growing but grew for less distance. At 2 months, both deflected and crushed fibers became much more stable. These results show that the morphology and behavior of fibers regenerating into the same target tissue can be substantially altered by the injury conditions, that is, they show state-dependent plasticity. The morphology and behavior of the deflected fibers suggest they were impaired in their capacity to grow to their correct targets.
Retinotectal maps: Molecules, models and misplaced data
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The mechanisms underlying the formation of topographic maps in the retinotectal system have long been debated. Recently, members of the Eph and ephrin receptor–ligand family have been found to provide a molecular substrate for one type of mechanism, that of chemospecific gradient matching, as proposed by Sperry. However, experiments over several decades have demonstrated that there is more to map formation than gradient matching. This article briefly reviews the old and new findings, argues that these two types of data must be properly integrated in order to understand map formation fully, and suggests some experimental and theoretical ways to begin this process.
Roger Sperry and his chemoaffinity hypothesis
1998, Neuropsychologia
In the early 1940s, Roger Sperry performed a series of insightful experiments on the visual system of lower vertebrates that led him to draw two important conclusions: When optic fibers were severed, the regenerating fibers grew back to their original loci in the midbrain tectum to re-establish a topographical set of connections; and the re-establishment of these orderly connections underlay the orderly behavior of the animal. From these conclusions, he inferred that each optic fiber and each tectal neuron possessed cytochemical labels that uniquely denoted their neuronal type and position and that optic fibers could utilize these labels to selectively navigate to their matching target cell. This inference was subsequently formulated into a general explanation of how neurons form ordered interconnections during development and became known as the chemoaffinity hypothesis. The origins of this hypothesis, the controversies that surrounded it for several decades and its eventual acceptance, are discussed in this article.

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¹: I thank Professor R. W. Sperry for his support of this work and for his constructive criticism of the manuscript. I am also indebted to Dr. K. I. Naka, Mr. P. Jonkhoff, Mr. R. Meyer, and Mrs. R. Johnson for their technical assistance. The research was supported by Grant MH 0337 from the U. S. Public Health Service and the author held a Postdoctoral Fellowship (2 FO2 NS 42760-02) from the National Institutes of Health.

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Reorganization of retinotectal projection following surgical operations on the optic tectum in goldfish

Abstract

Exp. Neurol.

Exp. Neurol.

Effect of forcing a regenerative optic nerve bundle towards a foreign region of the optic tectum

Anat. Rec.

Optic nerve regeneration after surgical cross-union of medial and lateral optic tracts

Amer. Zool.

Central routes taken by regenerating optic fibers

Physiologist

Units sensitive to direction of motion in goldfish optic tectum

Nature London

The representation of the retina on the optic lobe of the frog

Quart. J. Exp. Physiol.

Regeneration of the optic nerve in Xenopus laevis

Quart. J. Exp. Physiol.

A study of the retinotectal projection during regeneration of the optic nerve in the frog

Axial differences in the reinnervation of the optic tectum by regenerating optic nerve fibers

J. Physiol. London

Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibers

Exp. Brain Res.

Tungsten microelectrode for recording from single units

Science

The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count

Quart. J. Exp. Physiol.

Types of visual response from single units in the optic tectum and optic nerve of the goldfish

Quart. J. Exp. Physiol.