Movement through the Last Decade

Neurons, Networks, and Motor Behavior By Paul S. G. Stein, Sten Grillner, Allen I. Selverston, Douglas Stuart. Massachusetts: MIT Press Cambridge (1997). 305 pp. $60.00Even though studies of neuronal networks for movement do not move at the blistering speed of molecular biology, important advances still occur at a steady pace. This progress has been heralded in each of the last three decades by a symposium and a resulting book, organized and edited by leaders in the study of motor systems. Neurons, Networks, and Motor Behavior (Figure 1Figure 1) is the third of these books, reviewing work on motor circuitry over the last decade. The previous books in the series have been landmark books in motor control. They helped to define the state of the field in each decade and have held a prominent place on the book shelves of people both inside and outside of the area. This book follows in that strong tradition. In many ways, it is even better than those that came before.Figure 1The Book Cover from Neurons, Networks, and Behavior Reprinted with Permission from MIT PressView Large Image | View Hi-Res Image | Download PowerPoint SlideThe book emphasizes those systems in which motor circuits are reasonably well defined at a cellular level, including the brainstem and spinal cord of vertebrates and key model systems from invertebrates. Groups of chapters address major issues in motor control, such as the selection and initiation of motor patterns, rhythmogenesis, computational methods of study, and short- and long-term modulation of motor output by sensory and neuromodulatory systems.The book departs from the previous volumes, because the editors attempted to convince authors addressing similar issues in different systems to collaborate on individual chapters. The result is a book in which many of the chapters speak to the broader issues in motor control better than the past volumes. Where this approach works best is in chapters that show a true integration and comparison of the results from model systems. In a chapter by Pearson and Ramirez, for example, they provide a compelling account of how transmission in sensory pathways is modulated by the motor task and the phase of the ongoing movements in animals as different as cats, insects, and crustaceans. Other well-integrated, broadly comparative accounts in the book document the building blocks of vertebrate and invertebrate central pattern generators and the chemical modulation of motor circuits. Overall, this book is less a compilation of myopic, detailed views of particular systems and more of an integrative work, designed to present the principles of organization to be extracted from studies across species. This is no doubt a consequence of the effort of the editors to encourage collaboration among the authors.What, then, does the book reveal about the changes in our understanding of motor control over the past decade? There is the usual, gradual accretion of understanding of the details of particular circuits in both invertebrates and vertebrates. Although such accounts are essential as the foundation for extracting principles of motor control, the more important advances are those which change the way we think about circuits generally. These have occurred on several fronts and have in common the development of a much better appreciation for the dynamic aspects of motor circuits.The most fundamental change in our thinking is one that is clearly owed to the invertebrate models. This is the notion that circuits, as defined by anatomical connections, can be reconfigured in very dynamic ways to produce different motor outputs. This reconfiguration occurs through the action of neuromodulators upon the channels and synapses in the network, leading to changes in cellular properties and functional connectivity, which alter the circuit output. The fundamentals of these modulatory effects are well described in several chapters, which also document similar effects in both invertebrate and vertebrate systems. These neuromodulators can act not only on adult systems but also to restructure the functional properties of neurons and circuits in association with the changing demands on the motor systems during development. Here, as is often the case, the results from relatively crisp, clean invertebrate models have served to inform and guide the experiments of those working on the often murkier vertebrate systems.The book also documents the development of a much better appreciation of the dynamic aspects of the role of sensory input in motor behaviors. This includes such important discoveries as the ability of the nervous system to rapidly alter the throughput in different sensory reflex pathways. Gating of the sensory pathways allows for only the relevant sensory reflexes to participate in any particular motor behavior. Reflex pathways for postural control in a standing animal might not, for example, be appropriate during movement. The nervous system solves this problem by effectively matching the throughput in particular pathways to the motor task at hand. This can occur through such novel mechanisms as efferent affects on proprioceptors, presynaptic modulation of afferent pathways, and behavior-dependent neuromodulatory effects on transmission in reflex pathways.Over the past decade, computational modeling studies have become an integral part of motor control work. To a certain extent, this is linked to the recognition of the complexity of function that comes with the dynamic modulation of circuits at many levels of organization. Intuition alone is not enough to determine how the complex and changing interactions among different channel types, synapses, and neurons will influence the output of the motor circuits. The important roles that models play as aids to understanding and as guides for experimentation are clearly laid out in several of the chapters. The role of models is likely to increase still further over the next decade, because a strong interface between computational models and biology seems the only way that we will be able to understand complex networks and their links to behavior.The growing role of computational models is just one hint from the book of what is coming in the next decade. Another area that is sure to expand is the study of neuronal populations. One chapter of the book documents the coding by neuronal populations of saccadic eye movements in primates and bending and orientation movements in leeches and cockroaches. This is beautiful work, which reveals how neurons act as groups to determine the form of movements. Understanding the rules of coding by neuronal populations will prove essential for understanding vertebrate movements, all of which depend on populations of similar neurons. Many invertebrate systems involve populations too, although the focus has historically been directed at those invertebrate systems with small numbers of identifiable cells. Future studies of neuronal populations of manageable size in invertebrates and nonmammalian vertebrates will likely inform similar attempts to understand the huge populations in mammalian systems.Tighter links between circuits and behavior are ahead as well. The tendency has been toward the reduction of systems, with many studies of isolated bits of animals. This is still flourishing, as work on slice preparations grows. Such work is fundamental; indeed, accounts in the book show that slice work offers the best hope of understanding the circuits for rhythmic limb movements and breathing. Slices (and ganglia), however, do not behave. Ultimately, the aim is to understand the behavior of the whole animal, so we must eventually put the bits of the animal back together and see if we can explain its behavior. A few systems have reached a level of understanding in which this is becoming possible. One such attempt to build a “neuromechanical” model of a swimming lamprey is described in the modeling section of the book. Tighter, more realistic links to behavior are ahead, with the work over the next decade building on the foundations described so well in this book.