Neuronal Circuits That Generate Swimming Movements in Leeches

Swimming undulations in leeches arise from iterated segmental oscillators that are coupled by intersegmental interactions. Oscillator subunits, comprising individually identified intersegmental interneurons (INs) and local inhibitory motoneurons, control the activity of excitatory motoneurons that command body wall tension. Synaptic interactions within ganglia are almost exclusively non-spike-mediated; however, intersegmental connections, which together with sensory feedback from segmental muscle tension receptors set rostrocaudal phase lags, are mediated by impulses. The latter have an interganglionic transit time of about 15 ms. Overall, swimming in leeches is generated by local oscillators linked by individually weak, but in the aggregate strong, intersegmental interactions. Driven by an extensive set of multisegmental excitatory interneurons, the system functions as a unit.

Cochlear Nucleus

Neuronal circuits in the brainstem convert the output of the ear, which carries the acoustic properties of ongoing sound, to a representation of the acoustic environment that can be used by the thalamocortical system. Most important, brainstem circuits reflect the way the brain uses acoustic cues to determine where sounds arise and what they mean. The circuits merge the separate representations of sound in the two ears and stabilize them in the face of disturbances such as loudness fluctuation or background noise. Embedded in these systems are some specialized analyses that are driven by the need to resolve tiny differences in the time and intensity of sounds at the two ears and to resolve rapid temporal fluctuations in sounds like the sequence of notes in music or the sequence of syllables in speech.

Olfactory Bulb

The olfactory bulb is the site of the first synaptic processing of the olfactory input from the nose. It is present in all vertebrates (except cetaceans) and a the analogous antennal lobe in most invertebrates. With its sharply demarcated cell types and histological layers, and some well-studied synaptic interactions, it is one of the first and clearest examples of the microcircuit concept in the central nervous system. The olfactory bulb microcircuit receives the information in the sensory domain and transforms it into information in the neural domain. Traditionally, it has been considered analogous to the retina in processing its sensory input, but that has been replaced by the view that it is more similar to the thalamus or primary visual cortex in processing its multidimensional input. This chapter describes the main synaptic connections and functional operations and how they provide the output to the olfactory cortex

The Insect Visual System: Correspondence with Vertebrates and with Olfactory Processing

A 1915 monograph by the Nobel Prize–winning neuroanatomist Santiago Ramón y Cajal and Domingo Sánchez y Sánchez, describing neurons and their organization in the optic lobes of insects, is now standard fare for those studying the microcircuitry of the insect visual system. The work contains prescient assumptions about possible functional arrangements, such as lateral interactions, centrifugal pathways, and the convergence of neurons onto wider dendritic trees, to provide central integration of information processed at peripheral levels of the system. This chapter will consider further indications of correspondence between the insect-crustacean and the vertebrate visual systems, with particular reference to the deep organization of the optic lobe’s third optic neuropil, the lobula, and part of the lateral forebrain (protocerebrum) that receives inputs from it. Together, the lobula and lateral protocerebrum suggest valid comparison with the visual cortex and olfactory centers.

Subthalamo-Pallidal Circuit

The subthalamo-pallidal system constitutes the second layer of circuitry in the basal ganglia, downstream of the striatum. It consists of four nuclei. Two of them, the external segment of the globus pallidus (GPe) and subthalamic nucleus (STN), make their connections primarily within the basal ganglia. The others, the internal segment of the globus pallidus (GPi) and the substantia nigra pars reticulata (SNr), are the output nuclei of the basal ganglia. Collectively, their axons distribute collaterals to all the targets of the basal ganglia. Rare interneurons have been reported in each of them from studies of Golgi-stained preparations, but they have not so far been confirmed using more modern methods. The circuit as described here is based primarily on studies of the axonal arborizations of neurons stained individually by intracellular or juxtacellular labeling.

Templates for Neural Dynamics in the Striatum: Striosomes and Matrisomes

The striatum appears to be a relatively simple forebrain region compared to the overlying neocortex, with its horizontal layers and vertical columns. In fact, the striatum in mammals has a sophisticated architecture of its own. This large subcortical region is now suspected of having a major influence on how the neocortex carries out its own functions—even functions related to human language. Furthermore, abnormalities in the striatum are increasingly being discovered in human disorders affecting both cognitive and motor functions. It is, as a consequence, increasingly difficult to see the neocortex as a higher structure and the striatum as a lower structure in terms of their influence on behavior. The chapter is not a full review of this topic, but it points out some findings from the author’s laboratory that hint at such functions for the striosomal system.

Thalamocortical Networks

The thalamus and cerebral cortex are intimately linked through strong topographical connections, not only from the thalamus to the cortex, but also from the cortex back to the thalamus. As in many parts of the brain, the basic circuit of thalamocortical connectivity is relatively simple, although intracortical and corticocortical connectivity provides a high level of complexity. One of the basic operations of the thalamocortical network is the generation of rhythmic oscillations, which are now relatively well understood. In the normal brain, these thalamocortical oscillations typically occur during sleep, although their pathological counterparts may appear as seizures during sleep or waking. Unfortunately, the normal function of reciprocal thalamocortical connectivity during the waking state is still unknown. Even so, focused research is yielding insights into the properties of each of the cellular and synaptic components of these networks and how they interact to perform circuitwide operations.

Tadpole Swimming Network

Xenopus laevis frog tadpoles near the time of hatching have proved to be an excellent model system in which to explore the neural mechanisms responsible for the initiation, maintenance, sensory adaptation, and termination of rhythmic locomotor activity in vertebrates. The underlying neural network is one of the most completely understood in any vertebrate. Detailed knowledge has accrued over the last 40 years, highlighting conserved operational features of vertebrate rhythm generators and serving as an invaluable platform from which to investigate associated issues of fundamental importance in neuroscience, such as motor program switching, transmitter corelease, network development, neuromodulation, and metamodulation of network operation. There are many advantages of this simple model system, including the presence of a well-defined network output that relates directly to the behavior of the animal under study (namely, swimming locomotion).

Modularity and Modulation of Locomotor Circuits in Adult Vertebrates

The compartmentalized organization of the nervous system entails that specific functions are localized in different brain areas and regions of the spinal cord. Dedicated microcircuits in each region/area generate relevant motor behaviors by virtue of their connectivity and dynamic computations, combined with their ability to integrate internal and external cues. The patterns of motor actions are often versatile, with continuous change in speed and coordination as circumstances demand. How this versatility is encoded within microcircuits in the brain and spinal cord is a question that has been difficult to address. Although many mechanisms can contribute, two important tenets underlying this versatility are the modularity and modulation of microcircuits.

The Lamprey Postural Circuit

The lamprey has two principal behavioral states—a quiescent state, when it is attached to the substrate with its sucker mouth; and an active state, when it locomotes. It is capable of several forms of locomotion, but it actively stabilizes its body orientation in space only during the main form, fast forward swimming. During fast forward swimming, orientation of the lamprey in the sagittal (pitch) and transversal (roll) planes is stabilized in relation to the gravity vector by means of the postural control systems driven by vestibular input. Any deviations from the stabilized orientation are reflected in vestibular signals, which cause corrective motor responses. In the pitch and yaw planes, the corrections occur due to the body bending in the corresponding plane. In the roll plane, the corrections occur due to a change in the direction of locomotor body undulations, from lateral to oblique.