Invertebrate Neuroscience

The ability to sense and respond to a rewarding stimulus is a key advantage for animals in their natural environment. The circuits that mediate these responses are complex, and it has been difficult to identify the fundamental principles of reward structure and function. However, the well-characterized brain anatomy and sophisticated neurogenetic tools in Drosophila melanogaster make the fly an ideal model to understand the mechanisms through which reward is encoded. Drosophila find food, water, intoxicating substances, and social acts rewarding. Basic monoaminergic neurotransmitters, including dopamine (DA), serotonin (5-HT), and octopamine (OA), play a central role in encoding these rewards. DA is central to sensing, encoding, responding, and predicting reward, whereas 5-HT and OA carry information about the environment that influences DA circuit activity. In contrast, slower-acting neuromodulators such as hormones and neuropeptides play a key role in both encoding the pleasurable stimulus and modulating how the internal environment of the fly influences reward sensation and seeking. Recurring circuit motifs for reward signaling identified in Drosophila suggest that these key principles will help elucidate understanding of how reward circuits function in all animals.

The central complex (CX) is the only unpaired brain region of the insect brain. It is located at the interface of sensory processing and motor control and plays a vital role in context dependent action selection. The CX has four main tasks. First, the encoding of the insect’s orientation in space, i.e., the generation of an internal head direction signal based on both rotational self-motion and external sensory signals. Second, the generation of goal direction representations. Third, the selection of an appropriate goal direction based on context, internal state, and previous experience. And finally, the initiation of motor steering signals based on comparing heading direction and goal directions. The highly regular, almost crystalline neuroarchitecture of repeating computational elements provide the structural basis for these computations. These tight structure function relationships have revealed that the CX performs highly efficient, vector-based computations, in which vectors are encoded as sinusoidal activity patterns across populations of neurons. The deep insight into the computational algorithms implemented in this brain area have made the CX a prime model system to study the neural basis of context-dependent action selection and behavioral decisions, as well as the mechanisms of circuit evolution.

Color plays an important role in insect life—many insects forage on colorful flowers and/or have colorful bodies. Accordingly, most insects have multiple spectral types of photoreceptors in their eyes, which gives them the capability to see colors. However, insects cannot perceive colors in the same way as human beings do because their eyes and brains differ substantially. An insect was the first nonhuman animal whose ability to discriminate colors has been demonstrated - in the beginning of the 20th century, von Frisch showed that the honeybee, Apis mellifera, can discriminate blue from any shade of gray. This method, called the gray-card experiment, is an accepted “gold standard” for the proof of color vision in animals. Insect species differ in the combinations of photoreceptors in their eyes, with peak sensitivities in ultraviolet (UV) and/or blue, green, and sometimes red parts of the spectrum. The number of photoreceptor spectral types can be as little as one or two, as in the grasshopper Phlaeoba and the beetle Tribolium, and as many as 10 and more in some species of butterflies and dragonflies. However, not all spectral receptor types are necessarily used for color vison. For example, the butterfly Papilio xuthus uses only four of its eight photoreceptors for color vision. Some insects have separate channels for processing chromatic and achromatic (lightness) information. In the honeybee, the achromatic channel has high spatial resolution and is mediated only by long-wavelength sensitive, or “green,” photoreceptors alone, whereas the spatial resolution of chromatic vision is low and mediated by all three spectral types of photoreceptors. Whether other insects have a similar separation of chromatic and achromatic vision remains uncertain. In contrast to vertebrates, insects do not use distinct sets of photoreceptors for nocturnal vision, and some nocturnal insects can see color at night. Insect photoreceptors are inherently polarization sensitive because of their microvillar organization. Therefore, some insects cannot discriminate changes in polarization of light from changes in its spectral composition. However, many insects sacrifice polarization sensitivity to retain reliable color vision. For example, in the honeybee, polarization sensitivity is eliminated by twisting the rhabdom in most parts of its compound eye except for the dorsal rim area that is specialized in polarization vision. Insects experience color constancy and color-contrast phenomena. Although in humans these aspects of vision are often attributed to cortical processing of color, simple models based on photoreceptor adaptation may explain color constancy and color induction in insects. Color discriminations can be evaluated using a simple model, which assumes that it is limited by photoreceptor noise. This model can help to predict discrimination of colors that are ecologically relevant, such as flower colors for pollinating insects. However, despite the fact that many insects forage on flowers, there is no evidence that insect pollinator vision coevolved with flower colors. The diverse color vision in butterflies appears to adaptively facilitate the recognition of their wing colors.

The octopus, with its eight long and flexible arms, is an excellent example of the independent evolution of highly efficient motor behavior in a soft-bodied animal. Studies will be summarized to show that the amazing behavioral motor abilities of the octopus are achieved through a special embodied organization of its flexible body, unusual morphology, and a unique central and peripheral distribution of its extremely large nervous system. This special embodied organization of brain–body–environment reciprocal interactions makes it possible to overcome the difficulties involved in generation and control of movement in an animal, which unlike vertebrates and arthropods lacks rigid skeletal appendages.

Euopisthobranchia (Aplysia), Nudipleura (Tritonia, Hermissenda, Pleurobranchaea), and Panpulmonata (Lymnaea, Helix, Limax) gastropod mollusks exhibit a variety of reflex, rhythmic, and motivated behaviors that can be modified by elementary forms of learning and memory. The relative simplicity of their nervous systems and behavioral repertoires has allowed the uncovering of processes of neuronal and synaptic plasticity underlying non-associative learning, such as habituation, sensitization, and different forms of associative learning, such as classical and operant conditioning. Decades of work on these simpler and accessible animal systems have almost uniquely yielded an understanding into the mechanistic basis of learning and memory spanning behavior, neuronal circuitry, and molecules. Given the conservative nature of evolutionary processes, the mechanisms deciphered have also provided valuable insights into the neural basis of learning and memory in other metazoans, including higher vertebrates.

It is conceptually reasonable to explore how the evolution of behavior involves changes in neural circuitry. Progress in determining this evolutionary relationship has been limited in neuroscience because of difficulties in identifying individual neurons that contribute to the evolutionary development of behaviors across species. However, the results from the feeding systems of gastropod mollusks provide evidence for this concept of co-evolution because the evolution of different types of feeding behaviors in this diverse group of mollusks is mirrored by species-specific changes in neural circuitry. The evolution of feeding behaviors involves changes in the motor actions that allow diverse food items to be acquired and ingested. The evolution in neural control accompanies this variation in food and the associated changes in flexibility of feeding behaviors. This is present in components of the feeding network that are involved in decision making, rhythm generation, and behavioral switching but is absent in background mechanisms that are conserved across species, such as those controlling arousal state. These findings show how evolutionary changes, even at the single neuron level, closely reflect the details of behavioral evolution.

Visual camouflage change is a hallmark of octopus, squid, and cuttlefish and serves as their primary defense against predators. They can change their total body appearance in less than a second due to one principal feature: every aspect of this sensorimotor system is neurally refined for speed. Cephalopods live in visually complex environments such as coral reefs and kelp forests and use their visual perception of backgrounds to rapidly decide which camouflage pattern to deploy. Counterintuitively, cuttlefish have evolved a small number of pattern designs to achieve camouflage: Uniform, Mottle, and Disruptive, each with variation. The expression of these body patterns is based on several fundamental scene features. In cuttlefish, there appear to be several “visual assessment shortcuts” that enable camouflage patterning change in as little as 125 milliseconds. Neural control of the dynamic body patterning of cephalopods appears to be organized hierarchically via a set of lobes within the brain, including the optic lobes, the lateral basal lobes, and the anterior/posterior chromatophore lobes. The motor output of the central nervous system (CNS) in terms of the skin patterns that are produced is under sophisticated neural control of chromatophores, iridophores, and three-dimensional skin papillae. Moreover, arm postures and skin papillae are also regulated visually for additional aspects of concealment. This coloration system, often referred to as rapid neural polyphenism, is unique in the animal kingdom and can be explained and interpreted in the context of sensory and behavioral ecology.

The nematode, Caenorhabditis elegans (C. elegans), is an organism useful for the study of learning and memory at the molecular, cellular, neural circuitry, and behavioral levels. Its genetic tractability, transparency, connectome, and accessibility for in vivo cellular and molecular analyses are a few of the characteristics that make the organism such a powerful system for investigating mechanisms of learning and memory. It is able to learn and remember across many sensory modalities, including mechanosensation, chemosensation, thermosensation, oxygen sensing, and carbon dioxide sensing. C. elegans habituates to mechanosensory stimuli, and shows short-, intermediate-, and long-term memory, and context conditioning for mechanosensory habituation. The organism also displays chemotaxis to various chemicals, such as diacetyl and sodium chloride. This behavior is associated with several forms of learning, including state-dependent learning, classical conditioning, and aversive learning. C. elegans also shows thermotactic learning in which it learns to associate a particular temperature with the presence or absence of food. In addition, both oxygen preference and carbon dioxide avoidance in C. elegans can be altered by experience, indicating that they have memory for the oxygen or carbon dioxide environment they were reared in. Many of the genes found to underlie learning and memory in C. elegans are homologous to genes involved in learning and memory in mammals; two examples are crh-1, which is the C. elegans homolog of the cAMP response element-binding protein (CREB), and glr-1, which encodes an AMPA glutamate receptor subunit. Both of these genes are involved in long-term memory for tap habituation, context conditioning in tap habituation, and chemosensory classical conditioning. C. elegans offers the advantage of having a very small nervous system (302 neurons), thus it is possible to understand what these conserved genes are doing at the level of single identified neurons. As many mechanisms of learning and memory in C. elegans appear to be similar in more complex organisms including humans, research with C. elegans aids our ever-growing understanding of the fundamental mechanisms of learning and memory across the animal kingdom.

Although the Cnidaria have evolved a wide range of body forms matched with an equally varied neural anatomy, individual species exhibit common patterns of behavior. For example, in all species a key challenge for the nervous system is to transfer food from the peripherally mounted tentacles to the centrally located stomach. Foraging movements, necessary to maintain the food supply, must be accomplished in such a way as to avoid interference with the primary objective of getting prey into the mouth. Furthermore, the hunt for prey must be balanced by a measured response to “threat.” Different species respond to threat in markedly different ways, but in each case foraging is inhibited, just as it is during transmission of food. One hundred years ago, G. H. Parker questioned whether a centralized or a locally organized nervous system could best account for sea anemone behavior. Anatomical and electrophysiological studies now suggest that in most Cnidaria there is a degree of hierarchical control, with local reflexes coordinated by more condensed systems of neurons. This organization is highly developed in the nerve rings of hydrozoan medusae and takes the form of ganglion-like rhopalia in the Cubozoa. Even in hydrozoan polyps such as Hydra there are at least four separate neuronal systems. It is likely that the underlying mechanisms (containing both homologous and analogous elements) will be best revealed by a comparative approach that directly relates behavior with its molecular basis. Useful examples include comparisons between sea anemones with and without through-conducting systems; between hydra with and without oral rings; between medusae with and without coordinated escape swimming. Recent advances in transgenomic labeling have shown the way forward.