Control of Locomotion in Annelids

This article reviews the status of research on locomotion in segmented worms. It focuses on three major groups (leeches, earthworms, and nereid polychaetes) that have attracted the most research attention. All three groups show two types of locomotion: crawling (moving over a solid substrate) and swimming (moving through a liquid). The adults of all three groups form a hydroskeleton by controlling the pressure within the segments, and they locomote by controlling the shapes of the individual segments in coordinated spatial and temporal patterns. Many annelid larvae use cilia to move through water. Four aspects of the locomotory patterns are considered: the kinematics (the movement patterns), biomechanics (how muscle contractions produce movement), the neuronal basis of the movement patterns, and efforts to produce robots that move like annelid worms.

Rapid Neural Polyphenism in Cephalopods

Octopus, squid, and cuttlefish can change their appearance (phenotype) in 200–700 msec due to neural control of chromatophore organs, iridophore cells, and three-dimensional papillae in their elaborate skin. Great strides have been made in determining the primary visual background stimuli that guide camouflage skin patterning in cuttlefish, yet many key details remain unknown. The current behavioral/psychophysical experimental paradigm developed in cuttlefish needs to be expanded to octopus and squid, which will potentially elucidate general principles governing complex behaviors such as communication and camouflage. The neural underpinnings of this dynamic polyphenic system are poorly known. Peripheral control mechanisms of chromatophores and iridophores have been elucidated recently, but central nervous system experimentation has lagged far behind; both aspects require targeted neurobiological study, genomic approaches, and system modeling. The unusual neuroanatomy and complex behavior of these marine invertebrates provide an opportunity to discover novel mechanisms of visual perception, decision-making, and motor output.

Invertebrate Genomics Provide Insights Into the Origin of Synaptic Transmission

During the evolution of synapses, existing molecules were exapted to serve in specific synaptic roles. Recent increased availability of assembled transcriptomes from organisms that evolved before and after the appearance of the earliest synapses provides the opportunity to trace molecular adaptations important for development of fast synaptic transmission. We discuss issues that affect transcriptome assembly and phylogenetic analysis, and which therefore impact this analysis. We use relatively recent transcriptomes of pre-bilaterians to examine the molecular evolution of three types of critical synapse-specific proteins: vesicular transporters, synaptotagmins and ionotropic glutamate receptors. The results emphasize the fundamental difficulties in defining the specific point at which a protein “assumes” a synaptic function. Nevertheless, the analysis informs our understanding of several major evolutionary topics, including the evolution of synaptic vesicles and the identity of the first neurotransmitter used for fast, synchronous transmission. This analysis is also relevant for the current discussion of whether neuronal and synaptic function evolved separately, once in ctenophores and once in cnidarians and the main bilaterian lineage.

Rhythmic Pattern Generation in Invertebrates

This chapter begins by defining central pattern generators (CPGs) and proceeds to focus on one of their core components, the timing circuit. After arguing why invertebrate CPGs are particularly useful for the study of neuronal circuit operation in general, the bulk of the chapter then describes basic mechanisms of CPG operation at the cellular, synaptic, and network levels, and how different CPGs combine these mechanisms in various ways. Finally, the chapter takes a semihistorical perspective to discuss whether or not the study of invertebrate CPGs has seen its prime and what it has contributed—and may continue to offer—to a wider understanding of neuronal circuits in general.

Development of the Nervous System of Invertebrates

The complex architecture of the nervous system is the result of a stereotyped pattern of proliferation and migration of neural progenitors in the early embryo, followed by the outgrowth of nerve fibers along rigidly controlled pathways, and the formation of synaptic connections between specific neurons during later stages. Detailed studies of these events in several experimentally amenable model systems indicated that many of the genetic mechanisms involved are highly conserved. This realization, in conjunction with new molecular-genetic techniques, has led to a surge in comparative neurodevelopmental research covering a wide variety of animal phyla over the past two decades. This chapter attempts to provide an overview of the diverse neural architectures that one encounters among invertebrate animals, and the developmental steps shaping these architectures.

The Divergent Evolution of Arthropod Brains

Occasionally, fossils recovered from lower and middle Cambrian sedimentary rocks contain the remains of nervous system. These residues reveal the symmetric arrangements of brain and ganglia that correspond to the ground patterns of brain and ventral ganglia of four major panarthropod clades existing today: Onychophora, Chelicerata, Myriapoda, and Pancrustacea. Comparative neuroanatomy of living species and studies of fossils suggest that highly conserved neuronal arrangements have been retained in these four lineages for more than a half billion years, despite some major transitions of neuronal architectures. This chapter will review recent explorations into the evolutionary history of the arthropod brain, concentrating on the subphylum Pancrustacea, which comprises hexapods and crustaceans, and on the subphylum Chelicerata, which includes horseshoe crabs, scorpions, and spiders. Studies of Pancrustacea illustrate some of the challenges in ascribing homology to centers that appear to have corresponding organization, whereas Chelicerata offers clear examples of both divergent cerebral evolution and convergence.

Identifying Critical Genes, Neurotransmitters, and Circuits for Social Behavior in Invertebrates

This article examines the use of invertebrates to investigate the genetic and physiological mechanisms that regulate social behavior. A central goal in behavioral neuroscience is to understand how genes encode behavior and how environmental factors influence the expression of these relevant genes. In pursuit of this goal, many scientists who study behavior use a combined ecological, molecular, genomic, and physiological approach. This article discusses the distinct strengths of an approach, species, or finding in the context of two related but unique social behaviors: aggregation and aggression. It considers the genes that control aggregation and aggression by drawing on insights from C. elegans and Drosophila, respectively. It also describes the neurotransmitters, neuromodulators, and receptors that regulate aggregation and aggression.

Recent Trends in Invertebrate Neuroscience

This article presents a selective presentation of several notable trends in invertebrate neuroscience, which are intended to illustrate the central tenant that, essentially, basic invertebrate neuroscience and basic vertebrate neuroscience are converging to a remarkable degree. That is, the basic principles of cellular, network, and behavioral neuroscience are increasingly congruent within eukaryote phyla, with the notable exceptions of work that is explicitly clinical or concerned with pest control. The historical segregation of invertebrate and vertebrate neuroscience is of decreasing relevance and utility. An increasing literature has arisen that points out common structural and mechanistic themes across the invertebrate–vertebrate (IV) boundary. Among many examples, common neural circuit motifs play a causal role in decision-making circuits responsible for activating innate social behaviors in both Drosophila melanogaster and mice. Charles Darwin said, “It is absurd to talk of one animal being higher than another.” If some cephalopods are conscious, where do we draw the line?

Genetics of Behavior in C. elegans

The nematode Caenorhabditis elegans is among the most intensely studied animals in modern experimental biology. In particular, because of its amenability to classical and molecular genetics, its simple and compact nervous system, and its transparency to optogenetic recording and manipulation, C. elegans has been widely used to investigate how individual gene products act in the context of neuronal circuits to generate behavior. C. elegans is the first and at present the only animal whose neuronal connectome has been characterized at the level of individual neurons and synapses, and the wiring of this connectome shows surprising parallels with the micro- and macro-level structures of larger brains. This chapter reviews our current molecular- and circuit-level understanding of behavior in C. elegans. In particular, we discuss mechanisms underlying the processing of sensory information, the generation of specific motor outputs, and the control of behavioral states.

Associative Learning in Invertebrates

Behaviors of invertebrates can be modified by associative learning in a similar manner to those of vertebrates. Two simple forms of associative learning, Pavlovian and operant conditioning, allow animals to establish a predictive relationship between two events. Here we summarize five decades of studies of behavioral, cellular, and subcellular changes that are induced by these two learning paradigms in different invertebrate animal models. A comparative description of circuitry, neuronal elements, and properties that contribute to these conditioning procedures will be drawn to decipher common and distinguishing features of the learning processes. We will illustrate that similar circuits, synaptic and neuronal membrane plasticity, and similar molecular sites of detection of association are implicated in both forms of conditioning. However, evidence will also suggest that passively responding and endogenous dynamic properties of central networks and/or their constituent neurons might differentially contribute to Pavlovian and operant learning.