Editorial: models of invertebrate neurons in culture
In an attempt to better model the human nervous system, experimental preparations in current neuroscience have become increasingly complex: Advances in recording and imaging techniques as well as in analysis methods, enable the study of the mammalian nervous systems at a greater resolution than ever previously possible (e.g. Baker 2010; Stevenson and Kording 2011), and allows investigation of intricate phenomena in higher vertebrate models.
At the same time, however, with the renaissance of the notion of conserved principles in neurobiology (e.g. Ache and Young 2005; Marder and Bucher 2007; Hobert et al. 2010; see Greenspan 2005 and references within), there has been a revival of interest in invertebrate models in neuroscience. There are striking similarities between species in regard to basic neural features, from the nature of relevant proteins, to cellular processes, to the organization of neuronal networks and pathways, through neural computation and dynamic processes leading to behavior (e.g. Godenschwege et al. 2006; Yanay et al. 2008; Humeau et al. 2011; and see Lichtneckert and Reichert 2005; Arendt et al. 2008; Brand and Livesey 2011; for reviews). These common features span a phylogenetically broad array of animals, vertebrate and invertebrate alike, implying both common ancestors and optimal-homologue solutions to similar problems (Clarac and Pearlstein 2007; Humeau et al. 2011; Chittka and Skorupski 2011 and references within).
This special issue of the Journal of Molecular Histology combines and builds upon the different trends mentioned above by focusing on in vitro preparations of invertebrate neurons.
Neurons of various invertebrates in primary culture have served as the preparation of choice in numerous studies, focusing on nervous system development, form-function interactions, neural pharmacology and many more (e.g. Acklin and Nichlls 1990; Hayashi and Hildebrand 1990; Howes et al. 1991; Kirchhof and Bicker 1992; Lapied et al. 1993; Whitington 1993; Kloppenburg and Horner 1998; Fromherz 1999; and see current issue). Accordingly, these experimental preparations have made a major contribution to our current knowledge in these diverse fields. In vitro two-dimensional cultures of invertebrate neurons offer an attractive preparation for study, because of the large size of the cells and the facility with which they can be cultured under various conditions (e.g. extremely low densities). Furthermore, many invertebrate neurons are identifiable neurons (Leonard 2000), which allows identifying neurons in situ and the comparative characterization of neuronal structure and network circuitry in vitro (in culture) and in vivo.
This special issue provides a venue through which a panorama of current and cutting-edge neurobiological research is presented. Prospective authors with diverse research approaches were invited to contribute and we are delighted by the enthusiastic response. All submissions, including broad reviews, targeted reviews, and primary experimental papers were peer-reviewed. The result is a superb collection of articles, representing a wide variety of research areas with one thing in common, the important contribution of invertebrate neurons in culture as models in modern neuroscience.
Following is a short review of the contributions included in this special issue:
Schmold and Syed offer an in-depth review of the contribution of in vitro preparations from non-classical models (i.e. other than mouse, worm, or fly). Focusing largely on molluscs and leeches, the authors discuss learning, memory, and the concept of “identified” neurons, overall suggesting the advantages of using cultured invertebrate neurons as a model to study the fundamentals of nervous system function in higher animals.
Keeping to the mollusk neurons theme, Saada-Madar et al. present unusual features of the well-known pattern initiator neurons B31/B32 of Aplysia, when these neurons are cultured in isolation. The in vitro preparation assists in unveiling cellular properties and modulatory mechanisms, which are likely to contribute to the control of behavior in the animal.
An additional mollusk culture preparation, cultivated larval cells of the mussel Mytilus trossulus, is presented by Odintsova and Maiorova. These authors study cell adhesion and neuronal and muscle differentiation, and specifically the role of integrin-dependent mechanisms in these processes.
Insect neurons in culture have been amply studied and are accordingly well represented here. Ellen and Mercer review results obtained from studies of cultured insect antennal lobe neurons, suggesting an important modulatory role of the biogenic amines, dopamine and serotonin, in the regulation of neuronal development and promotion of cellular and behavioral plasticity.
Locusts are a leading preparation in the study of many neurophysiology and neuro-endocrinology-related questions. Locust neurons in culture have been used to investigate various questions of nervous system development, from cellular, and even molecular, to network-level aspects. The paper by Weigel et al. offers an important further step, presenting the locust primary neuronal culture as a model for the study of synaptic transmission.
Saad and Ayali report their results promoting a Drosophila primary neural culture preparation as a promising platform for studying a variety of processes related to nervous system development, activity, and pathology. The very well characterized in vitro network development, together with the well-known advantages offered by fly genetics, has great potential for future work.
Last but not least, further extending the presented repertoire of invertebrate models, Baranes et al. present a culture preparation of leech neurons plated on substrates photolithography-fabricated with repeatable nano-scale line-patterned ridges. Using high resolution electron microscopy, they demonstrate interactions of the neuronal processes with the nano-cues that affect neuronal morphology and neuronal branching topology.
To conclude, the varied collection of articles in this special issue offer readers the opportunity to be introduced to a diversity of research interests, methodologies, and approaches. The common theme or thread connecting these different contributions and research groups is a strong belief in the important contribution of invertebrate neurons in culture preparations to contemporary neuroscience.
I appreciate the timely submission of interesting manuscripts by the contributors. I am grateful to Martijn Roelandse and Srilakshmi Patrudu for invaluable help in assembling this special Issue.
- Hayashi JH, Hildebrand JG (1990) Insect olfactory neurons invitro—morphological and physiological characterization of cells from the developing antennal lobes of Manduca sexta. J Neurosci 10:848–859Google Scholar
- Howes EA, Cheek TR, Smith PJS (1991) Long-term growth in vitro of isolated, fully differentiated neurones from the central nervous system of an adult insect. J Exp Biol 156:591–605Google Scholar
- Kirchhof B, Bicker G (1992) Growth properties of larval and adult locust neurons in primary cell culture. J Comp Neurol 323:411–422Google Scholar
- Kloppenburg P, Horner M (1998) Voltage-activated currents in identified giant interneurons isolated from adult crickets Gryllus bimaculatus. J Exp Biol 201:2529–2541Google Scholar
- Lapied B, Tribut F, Sinakevitch I, Hue B, Beadle DJ (1993) Neurite regeneration of long-term cultured adult insect neurosecretory-cells identified as dum neurons. Tissue Cell 25:893–906Google Scholar
- Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric ganglion of lobsters and crabs. Annu Rev Physiol 69:291–316Google Scholar
- Shefi O, Ben-Jacob E, Ayali A (2002) Growth morphology of two-dimensional insect neural networks. Neurocomputing 44–46:635–643Google Scholar
- Whitington PM (1993) Axon guidance factors in invertebrate development. Pharmacol Ther 58:263–299Google Scholar