CONEUR 1560 1–2
Available online at www.sciencedirect.com
ScienceDirect Editorial overview: Motor circuits and action Ole Kiehn and Mark M Churchland Current Opinion in Neurobiology 2015, 33:xx–yy
http://dx.doi.org/10.1016/j.conb.2015.06.004 0959-4388/Published by Elsevier Ltd.
Ole KiehnPhD, MD Mammalian Locomotor Laboratory, Department of Neuroscience, Karolinska Institutet, Retziusva¨g 8, 17177 Stockholm, Sweden e-mail: [email protected] Ole Kiehn received his MD in 1985 and PhD in 1990 from University of Copenhagen, Denmark. He was a postdoctoral fellow at Cornell University, US. Presently he is a Professor of Neuroscience at the Department of Neuroscience at Karolinska Institutet. His laboratory attempts to understand mechanisms by which neurons and neural networks operate to generate movements. In particular, his work has focused on the molecular, cellular and network organization of spinal locomotor circuitries, their development and central control in mammals.
Mark M ChurchlandPhD Department of Neuroscience, Grossman Center for the Statistics of Mind, David Mahoney Center for Brain and Behavior Research, Kavli Institute for Brain Science, Columbia University Medical Center, New York, NY 10032, United States e-mail: [email protected] Mark Churchland received his PhD studying vision and oculomotor behavior at the University of California San Francisco. His postdoctoral work in the Neural Prosthetic Systems Laboratory at Stanford University focused on the cortical basis of movement preparation and execution, and upon the relationship of neural variability to behavioral outputs and sensory inputs. Presently, he is an Assistant Professor in the Department of Neuroscience at Columbia University Medical Center and the co-director of the Grossman Center for the Statistics of Mind. His laboratory focuses on the neural dynamics that underlie voluntary movement.
A trite but true observation is that the principle purpose of the central nervous system is to produce intelligent behavior. It therefore comes as no surprise that the study of motor control is central to the endeavor of understanding the brain, and intersects with the study of many other neural faculties including sensation, cognition and learning. The articles contained within this volume thus span a broad range of topics. Movement is both limited and guided by what is innately available in key locomotor circuits and by how that repertoire is accessed by other brain areas. The theme of how higher-level structures interact with lower-level structures thus appears often. Giszter describes how motor primitives both facilitate and constrain behavior by providing a set of available ‘building blocks’ that may be accessed in stereotyped and novel ways. Jin and Costa explore how interactions between cortex and the basal ganglia result in ‘chunking’ elements into action sequences via learning. Silberberg and Bolam detail new discoveries regarding the circuitries of the basal ganglia, in terms of both its diversity of internal connections, intrinsic modulation and connections from other brain areas. Grillner and Robertson describe how the basic neuronal organization of the basal ganglia is conserved throughout the vertebrate kingdom and outline a general circuit scheme for motor selection through downstream inhibitory control exerted by the basal ganglia over targets in the brainstem. A similar theme emerges in the context of locomotion, which is subserved in large part by spinal circuitry, or local circuitry in the case of invertebrates, yet is modulated and controlled by descending commands. Drew and Marigold discuss the cortical control of locomotion, particularly the contribution of primary motor cortex to the control of synergies of muscles and the involvement of posterior parietal cortex in planning gait modifications guided by visual cues. Perrier and Cotel discuss the rich repertoire of modulation of spinal motor circuits by serotonin and a novel involvement of the activation of extra-synaptic receptors. An emergent theme that appears from studies of spinal motor networks as highlighted by McLean and Dougherty is the modular and speed dependent organization of the vertebrate spinal locomotor network and the delineation of rhythm and pattern generation circuits. A speed dependent and task dependent organization of descending and local circuitries is also explored by Borgmann and Bu¨schges who additionally review the methodological advances that have revealed the fine control of locomotor networks in insects. For most behaviors the study of motor control is inexorably linked with the study of the sensory signals that initiate and guide movement. Indeed, in many cases the sensory system is an indispensable limb supporting the
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Current Opinion in Neurobiology 2015, 33:1–2
Please cite this article in press as: Kiehn O, Churchland MM: Editorial overview: Motor circuits and action, Curr Opin Neurobiol (2015), http://dx.doi.org/10.1016/j.conb.2015.06.004
CONEUR 1560 1–2
2 Motor circuits and action
dynamics that drive movement. Lisberger and Medina review one such case — the smooth pursuit system — where the impact of sensory variability can be traced through the entire pathway and produces most of the measured movement variability. Scott et al. similarly stress the central role of spinal and cortical feedback loops, the latter of which can subserve goal-directed responses at surprisingly short latencies. The role of feedback is, both intuitively and in many computational models, tied to the role of ‘efference copy’ signals that encode the feedback the motor system expected. In the context of skilled forelimb movements Azim and Alstermark provide new insights — using mouse genetic and behavioral studies — into the organization of spinal circuitries that provides a potential implementation of efference copy mechanisms, allowing a copy of descending motor commands a route back to cortex and the cerebellum. Therrien and Bastian illustrate that deficits following cerebellar damage support the hypothesis that the cerebellum does indeed use a predictive model: one that incorporates knowledge of limb dynamics. Similarly underscoring the importance of efference-copy feedback, Schneider and Mooney discuss the circuitry and function of corollary discharge signals in the auditory system of the mouse and songbird. Houde and Chang describe experiments that test predictions from a model of speech motor control that includes both sensory and predictive feedback. Because the role of cognition is to guide behavior, one expects many interactions between cognitive and motor computations. Sometimes these occur in surprising ways. Wang and Munoz describe how pupil dilation occurs not only in response to light, but also shows an ‘orienting response’ that is modulated by stimulus salience. Georgopoulos and Carpenter argue that a higher-level representation of reach direction is a fundamental principle of neural coding and prosthetic decoding, and discuss cognitive roles of motor cortex. Few motor circuits could perform well without the ability to adapt. Brownstone et al. discuss the spinal plasticity underlying motor learning and propose several interneuron-motor neuron circuit architectures as fundamental learning modules in the spinal cord. Huberdeau et al. review how careful behavioral measurements can be used to decompose motor adaptation into a fast, implicit component and a slow, explicit component. Learning, and the structures that normally implement it, are also of deep relevance to a number of clinical applications. Ethier et al. review work raising the possibility that neurally controlled muscle stimulation can induce beneficial plasticity in patients with motor deficits. Plotkin and Surmeier discuss the circuit and synaptic basis of Huntington’s
Current Opinion in Neurobiology 2015, 33:1–2
disease, in which corticostriatal signaling becomes progressively impaired, leading to a hypo-excitable disorder contrary to the expectations of many standard models of the disease. Ultimately the study of motor control seeks to link circuit level knowledge with computational properties that provide a mechanistic explanation of how the system does its job. To this end, Zhen and Samuel tie circuit structure to systems-level behavior in an organism — Caenorhabditis elegans — where the full map of connections is mostly known, but where questions about how behaviors are generated by neuronal circuits still remain. Witter and De Zeeuw describe how cerebellar modules have response properties tailored to the functions of the areas with which they interconnect. Murakami and Mainen discuss emerging conceptions of how neural activity evolves during decision making and movement preparation, laying out a framework in which function is understood using a combination of modern analysis methods, network modeling, and circuit-level dissection. A common theme of most of the work described above is that brain areas must interact and communicate to allow coordinated action. To better map the scope of interacting areas, Gallivan and Culham describe how new analysis techniques allow fMRI-based mapping of the broad network of areas involved in human motor control. With the goal of understanding how such areas interact, BattagliaMayer et al. review the influence of the timing of neural activity on the communication between cortical areas. Together these articles paint a portrait of a motor system that spans many components of the nervous system, yet still somehow manages to act as a holistic entity that produces sensible behavior serving the needs of the animal. It is fair to say that in most cases we still do not fully comprehend the nature of the key computational processes, nor how they are instantiated in the underlying circuitry. Yet the themes touched upon in this issue are those that arise again and again. The motor system is limited by the neuronal hardware, yet possesses a remarkable capacity to adaptively recruit that hardware. Movements can be produced and sustained by dedicated circuits, yet frequently depend critically on feedback, and the ability to anticipate feedback. Learning is ever-present, and both modifies existing behaviors and creates new behavioral sequences. Finally, modeling serves as a powerful tool for linking all the appropriate levels, and explaining how circuit-level features produce the population-level properties that in turn subserve systems-level computations.
Conflict of interest statement Nothing declared.
www.sciencedirect.com
Please cite this article in press as: Kiehn O, Churchland MM: Editorial overview: Motor circuits and action, Curr Opin Neurobiol (2015), http://dx.doi.org/10.1016/j.conb.2015.06.004
Available online at www.sciencedirect.com
ScienceDirect Editorial overview: Motor circuits and action Ole Kiehn and Mark M Churchland Current Opinion in Neurobiology 2015, 33:xx–yy
http://dx.doi.org/10.1016/j.conb.2015.06.004 0959-4388/Published by Elsevier Ltd.
Ole KiehnPhD, MD Mammalian Locomotor Laboratory, Department of Neuroscience, Karolinska Institutet, Retziusva¨g 8, 17177 Stockholm, Sweden e-mail: [email protected] Ole Kiehn received his MD in 1985 and PhD in 1990 from University of Copenhagen, Denmark. He was a postdoctoral fellow at Cornell University, US. Presently he is a Professor of Neuroscience at the Department of Neuroscience at Karolinska Institutet. His laboratory attempts to understand mechanisms by which neurons and neural networks operate to generate movements. In particular, his work has focused on the molecular, cellular and network organization of spinal locomotor circuitries, their development and central control in mammals.
Mark M ChurchlandPhD Department of Neuroscience, Grossman Center for the Statistics of Mind, David Mahoney Center for Brain and Behavior Research, Kavli Institute for Brain Science, Columbia University Medical Center, New York, NY 10032, United States e-mail: [email protected] Mark Churchland received his PhD studying vision and oculomotor behavior at the University of California San Francisco. His postdoctoral work in the Neural Prosthetic Systems Laboratory at Stanford University focused on the cortical basis of movement preparation and execution, and upon the relationship of neural variability to behavioral outputs and sensory inputs. Presently, he is an Assistant Professor in the Department of Neuroscience at Columbia University Medical Center and the co-director of the Grossman Center for the Statistics of Mind. His laboratory focuses on the neural dynamics that underlie voluntary movement.
A trite but true observation is that the principle purpose of the central nervous system is to produce intelligent behavior. It therefore comes as no surprise that the study of motor control is central to the endeavor of understanding the brain, and intersects with the study of many other neural faculties including sensation, cognition and learning. The articles contained within this volume thus span a broad range of topics. Movement is both limited and guided by what is innately available in key locomotor circuits and by how that repertoire is accessed by other brain areas. The theme of how higher-level structures interact with lower-level structures thus appears often. Giszter describes how motor primitives both facilitate and constrain behavior by providing a set of available ‘building blocks’ that may be accessed in stereotyped and novel ways. Jin and Costa explore how interactions between cortex and the basal ganglia result in ‘chunking’ elements into action sequences via learning. Silberberg and Bolam detail new discoveries regarding the circuitries of the basal ganglia, in terms of both its diversity of internal connections, intrinsic modulation and connections from other brain areas. Grillner and Robertson describe how the basic neuronal organization of the basal ganglia is conserved throughout the vertebrate kingdom and outline a general circuit scheme for motor selection through downstream inhibitory control exerted by the basal ganglia over targets in the brainstem. A similar theme emerges in the context of locomotion, which is subserved in large part by spinal circuitry, or local circuitry in the case of invertebrates, yet is modulated and controlled by descending commands. Drew and Marigold discuss the cortical control of locomotion, particularly the contribution of primary motor cortex to the control of synergies of muscles and the involvement of posterior parietal cortex in planning gait modifications guided by visual cues. Perrier and Cotel discuss the rich repertoire of modulation of spinal motor circuits by serotonin and a novel involvement of the activation of extra-synaptic receptors. An emergent theme that appears from studies of spinal motor networks as highlighted by McLean and Dougherty is the modular and speed dependent organization of the vertebrate spinal locomotor network and the delineation of rhythm and pattern generation circuits. A speed dependent and task dependent organization of descending and local circuitries is also explored by Borgmann and Bu¨schges who additionally review the methodological advances that have revealed the fine control of locomotor networks in insects. For most behaviors the study of motor control is inexorably linked with the study of the sensory signals that initiate and guide movement. Indeed, in many cases the sensory system is an indispensable limb supporting the
www.sciencedirect.com
Current Opinion in Neurobiology 2015, 33:1–2
Please cite this article in press as: Kiehn O, Churchland MM: Editorial overview: Motor circuits and action, Curr Opin Neurobiol (2015), http://dx.doi.org/10.1016/j.conb.2015.06.004
CONEUR 1560 1–2
2 Motor circuits and action
dynamics that drive movement. Lisberger and Medina review one such case — the smooth pursuit system — where the impact of sensory variability can be traced through the entire pathway and produces most of the measured movement variability. Scott et al. similarly stress the central role of spinal and cortical feedback loops, the latter of which can subserve goal-directed responses at surprisingly short latencies. The role of feedback is, both intuitively and in many computational models, tied to the role of ‘efference copy’ signals that encode the feedback the motor system expected. In the context of skilled forelimb movements Azim and Alstermark provide new insights — using mouse genetic and behavioral studies — into the organization of spinal circuitries that provides a potential implementation of efference copy mechanisms, allowing a copy of descending motor commands a route back to cortex and the cerebellum. Therrien and Bastian illustrate that deficits following cerebellar damage support the hypothesis that the cerebellum does indeed use a predictive model: one that incorporates knowledge of limb dynamics. Similarly underscoring the importance of efference-copy feedback, Schneider and Mooney discuss the circuitry and function of corollary discharge signals in the auditory system of the mouse and songbird. Houde and Chang describe experiments that test predictions from a model of speech motor control that includes both sensory and predictive feedback. Because the role of cognition is to guide behavior, one expects many interactions between cognitive and motor computations. Sometimes these occur in surprising ways. Wang and Munoz describe how pupil dilation occurs not only in response to light, but also shows an ‘orienting response’ that is modulated by stimulus salience. Georgopoulos and Carpenter argue that a higher-level representation of reach direction is a fundamental principle of neural coding and prosthetic decoding, and discuss cognitive roles of motor cortex. Few motor circuits could perform well without the ability to adapt. Brownstone et al. discuss the spinal plasticity underlying motor learning and propose several interneuron-motor neuron circuit architectures as fundamental learning modules in the spinal cord. Huberdeau et al. review how careful behavioral measurements can be used to decompose motor adaptation into a fast, implicit component and a slow, explicit component. Learning, and the structures that normally implement it, are also of deep relevance to a number of clinical applications. Ethier et al. review work raising the possibility that neurally controlled muscle stimulation can induce beneficial plasticity in patients with motor deficits. Plotkin and Surmeier discuss the circuit and synaptic basis of Huntington’s
Current Opinion in Neurobiology 2015, 33:1–2
disease, in which corticostriatal signaling becomes progressively impaired, leading to a hypo-excitable disorder contrary to the expectations of many standard models of the disease. Ultimately the study of motor control seeks to link circuit level knowledge with computational properties that provide a mechanistic explanation of how the system does its job. To this end, Zhen and Samuel tie circuit structure to systems-level behavior in an organism — Caenorhabditis elegans — where the full map of connections is mostly known, but where questions about how behaviors are generated by neuronal circuits still remain. Witter and De Zeeuw describe how cerebellar modules have response properties tailored to the functions of the areas with which they interconnect. Murakami and Mainen discuss emerging conceptions of how neural activity evolves during decision making and movement preparation, laying out a framework in which function is understood using a combination of modern analysis methods, network modeling, and circuit-level dissection. A common theme of most of the work described above is that brain areas must interact and communicate to allow coordinated action. To better map the scope of interacting areas, Gallivan and Culham describe how new analysis techniques allow fMRI-based mapping of the broad network of areas involved in human motor control. With the goal of understanding how such areas interact, BattagliaMayer et al. review the influence of the timing of neural activity on the communication between cortical areas. Together these articles paint a portrait of a motor system that spans many components of the nervous system, yet still somehow manages to act as a holistic entity that produces sensible behavior serving the needs of the animal. It is fair to say that in most cases we still do not fully comprehend the nature of the key computational processes, nor how they are instantiated in the underlying circuitry. Yet the themes touched upon in this issue are those that arise again and again. The motor system is limited by the neuronal hardware, yet possesses a remarkable capacity to adaptively recruit that hardware. Movements can be produced and sustained by dedicated circuits, yet frequently depend critically on feedback, and the ability to anticipate feedback. Learning is ever-present, and both modifies existing behaviors and creates new behavioral sequences. Finally, modeling serves as a powerful tool for linking all the appropriate levels, and explaining how circuit-level features produce the population-level properties that in turn subserve systems-level computations.
Conflict of interest statement Nothing declared.
www.sciencedirect.com
Please cite this article in press as: Kiehn O, Churchland MM: Editorial overview: Motor circuits and action, Curr Opin Neurobiol (2015), http://dx.doi.org/10.1016/j.conb.2015.06.004
