Elsevier

Brain Research Reviews

Volume 54, Issue 1, April 2007, Pages 113-161
Brain Research Reviews

Review
Invertebrate preparations and their contribution to neurobiology in the second half of the 20th century

Dedicated to all the pioneers mentioned in this review who have used invertebrate preparations to contribute greatly to our knowledge of neurobiology.
https://doi.org/10.1016/j.brainresrev.2006.12.007Get rights and content

Abstract

This review summarizes the contribution to neurobiology achieved through the use of invertebrate preparations in the second half of the 20th century. This fascinating period was preceded by pioneers who explored a wide variety of invertebrate phyla and developed various preparations appropriate for electrophysiological studies. Their work advanced general knowledge about neuronal properties (dendritic, somatic, and axonal excitability; pre- and postsynaptic mechanisms). The study of invertebrates made it possible to identify cell bodies in different ganglia, and monitor their operation in the course of behavior. In the 1970s, the details of central neural circuits in worms, molluscs, insects, and crustaceans were characterized for the first time and well before equivalent findings were made in vertebrate preparations. The concept and nature of a central pattern generator (CPG) have been studied in detail, and the stomatogastric nervous system (STNS) is a fine example, having led to many major developments since it was first examined. The final part of the review is a discussion of recent neuroethological studies that have addressed simple cognitive functions and confirmed the utility of invertebrate models. After presenting our invertebrate “mice,” the worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster, our conclusion, based on arguments very different from those used fifty years ago, is that invertebrate models are still essential for acquiring insight into the complexity of the brain.

Introduction

It is generally accepted that by the early 1970s, most of the separate disciplines investigating the central nervous system (CNS) converged to form an interdisciplinary endeavor called “neuroscience” (Neurobiology, a discipline devoted mainly to cellular mechanisms underlying behavior, can be considered a branch of neuroscience). In the second half of the 20th century, invertebrate neurobiology has figured prominently in the endeavor, with invertebrate preparations providing the means to explore many key mechanisms of neuronal function. This golden age of invertebrates has been celebrated by symposia and books (e.g., Fessard and Monnier, 1957, Florey, 1961, Bullock and Horridge, 1965, Wiersma, 1967, Usherwood and Newth, 1972, Salanki, 1973, Hoyle, 1977, Roberts and Roberts, 1983, Bush and Clarac, 1985, Barnes and Gladden, 1986, Gewecke and Wendler, 1985, Armstrong and Bush, 1991, Reichert, 1992) and by a large number of reviews (see below).

Work on invertebrates has been conducted using two different approaches. Many leaders in the field have worked on both vertebrates and invertebrates; for example Edgar Douglas Adrian (1889–1977), Albrecht Bethe (1872–1954), Theodore Holmes Bullock (1915–2005), Alfred Fessard (1900–1982), Ernst Florey (1927–1997), Erich von Holst (1908–1962), Bernard Katz (1911–2003), Stephen Kuffler (1913–1980), and even John Carew Eccles (1903–1997), together with others still doing so today. The belief of these scientists has been that results from the two groups of animals can be compared, despite their very different rankings on the evolutionary scale. The second approach is based on the belief that the rules of neural organization differ between vertebrates and invertebrates, and that a comparative, reductionist approach is unsuitable for a general application of concepts. While some behavioral capabilities exist only in humans or higher mammals and clearly require unique types of neuronal organization, we suggest that behavior is so general that common patterns of neuronal organization probably exist. “It must be admitted that the existence of common behavioral capabilities in man and higher invertebrates does not (necessarily) mean that common neuronal mechanisms are involved; it does however suggest that the mechanisms may be general and should be explored fully in whatever preparation they can be studied most effectively” (Kandel and Kupfermann, 1970, p. 194).

A similar but stronger argument was presented by Kuffler and Nicholls (1976) in the preface to their book: “Fortunately, in the brains of all animals that have been studied, there is apparent uniformity of principles for neurological signalling. Therefore, with luck, examples from a lobster or a leech will have relevance for our own nervous system.”(p. VIII).

In this historical review, our purpose is to highlight the key contributions of studies on invertebrates by focusing on the emergence of concepts that arose from the use of such preparations. By comparing information accumulated on each family of invertebrates, the power of these models becomes apparent, showing that they have given a significant boost to our understanding of neuronal functioning. The intention is not to compare the full range of data with data from observations of vertebrates. Quite the contrary, we are well aware that both vertebrate and invertebrate have contributed in a complementary manner. In most cases, neuronal properties hypothesized for invertebrates have been confirmed, albeit later, in vertebrates. Our present effort to summarize the invertebrate period is not be an exhaustive review. Rather, we discuss some of the most significant animal preparations that gave rise to selected new concepts, several of which are still being refined. To this end we focus on five topics:

  • 1.

    Modern-day pioneers in the field of invertebrate neurobiology and their animal preparations, which have been used extensively since the 1950s and 1960s.

  • 2.

    Some of the major contributions of the same pioneers to neurobiological knowledge and the general understanding of neuronal properties including the separate parts of the neuron (dendrites, soma, axon, dendrites, and synapse).

  • 3.

    Neural ganglia, their anatomical and physiological descriptions, and the analysis of simple input-output functions, including the “restricted network” concept of Kennedy et al. (1969).

  • 4.

    Motor behavior patterns, focusing on the central organization of certain rhythmic preparations and the concept of central pattern generators (CPGs), and how subsequent research has changed the meaning of this term.

  • 5.

    The analysis of highly complex behavior patterns, first in terms of selected neuronal operations and specific neuromodulatory neurons, and later relations between neuronal functions and behavioral mechanisms.

Recent studies on invertebrates have provided insights relevant to cognitive processes in the more developed brains of vertebrates. Some would question whether research on invertebrates is still relevant given advances in molecular biology, genetics, and cognitive science. We show below, however, that while the current situation differs greatly from that 50 years ago, much is still to be gained from research on invertebrates (Kandel, 2001, Marder et al., 2005).

Section snippets

Pioneers in the use of invertebrate preparations

By the mid 20th century, neurobiology was in total mutation. The first part of the century was dominated by four outstanding scientists who shared two Nobel prizes. In 1906, Camillo Golgi (1843–1926) and Santiago Ramon y Cajal (1852–1934) received their award for their anatomical and histological work on the basic structure of the nervous system. The most important contribution on the neuron doctrine was from Ramon y Cajal. In his first published article based on the results he obtained with

Neuronal properties of identified neurons

The neuron as perceived in the mid-20th century was depicted in a diagram by Harry Grundfest (1904–1983). It detailed the receptive inputs and central part that could initiate spikes and conduct them to the terminal output portion of the cell (1957, see Fig. 2A). The neuron was considered as to be a linear structure responding through an all-or-none process. This diagram was very popular and it was included in most textbooks published at the time. A similar approach is seen in the work of

Restricted networks and their actions

Most invertebrate preparations were developed because their neural networks contained a small number of neurons. This resulted in several advantages. It was possible to locate cell bodies inside ganglia and to produce an initial form of “neurogeography” (Kennedy et al., 1969) showing a small number of INs able to control selected hierarchical behaviors. Cells were identified as contributing to restricted circuits supporting a stereotyped behavior through reflex modulation.

The concept of central pattern generator

The “boom” of invertebrate preparations in this period from the mid 1960s to the 80s was spectacular. When properly dissected, most ganglia displayed auto-rhythmicity in their recorded outputs. This seems to confirm very early findings from Graham Brown (1911, 1914) on the cat spinal cord. Sometimes an easy form of activation, using classical neurotransmitters or electrical stimulation, was needed. Demonstrations with all these preparations showed that central circuits could produce a coherent

Neuronal circuits towards cognitive functions

We have seen that invertebrate preparations in this “golden age” were studied as “simple systems” analyzing certain cellular mechanisms in identified neurons. But more and data suggested that these networks were not so simple. In 1972, Usherwood organized a meeting on “Simple Nervous System” and his closing address confirms the complexity of these models. We shall now analyze complex behavioral functions and their neuronal mechanisms in invertebrate preparations.

The diversity of the anatomical

Conclusions

Invertebrate preparations made the second half of the 20th century a very fruitful period of progress in neurobiological science (Bullock, 1993, Chase, 2002, Gewecke and Wendler, 1985, Krasne and Glanzman, 1995, Kristan et al., 2005, Wiese et al., 1990, Wiese, 2002b, Wiese, 2002a) contributing to swift development in our knowledge, not only on the basic fundamental neuronal structures, but also on elaborated network functioning. The use of invertebrate models in parallel with lower vertebrate

Acknowledgments

We thank D. Cattaert and P. Meyrand for their comments on an early version of the manuscript. We appreciated also very much the extensive analysis and the suggested corrections made by the two referees. We would like to thank Miss Shan Benson for correcting the English version of the manuscript.

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