5421
J Physiol 591.22 (2013) pp 5421–5423
Neural circuits in movement control Henrik J¨orntell Neural Basis for Sensorimotor Control, Department of Experimental Medical Science, Lund University, Lund, Sweden Email: [email protected]
A symposium on neural circuits in movement control took place at Trolleholm Castle near Lund on May 27–28, 2011 (Fig. 1). The meeting was a celebration of the
lifetime achievements of Carl-Fredrik Ekerot, who is now retired. The meeting drew together participants from many different disciplines of motor systems neuroscience, but with a focus on the cerebellum and the spinocerebellar systems, which was the main field of interest of Carl-Fredrik Ekerot. Ekerot pioneered the field of climbing fibre microzones in the forelimb area of the C3 zone (Ekerot & Larson, 1980; Ekerot et al. 1991) and the role of the microzones as a functional unit in the cerebellar cortex and in the cerebellar nuclei (Garwicz & Ekerot, 1994;
Ekerot et al. 1995). He provided early evidence of the congruence between mossy fibre and climbing fibre inputs in the cerebellar cortex (Ekerot & Larson, 1973, 1980; Garwicz et al. 1998), made important contributions to early work on cerebellar plasticity research centred on the classical climbing fibre-dependent LTD of parallel fibre synapses on Purkinje cells (Ekerot & Kano, 1985, 1989), later discovering several new forms of plasticity between the parallel fibres and the interneurons and Purkinje cells (Ekerot & Jorntell, 2001; Jorntell & Ekerot, 2002), and made a unique and
The Journal of Physiology
Neuroscience
EDITORIAL
Figure 1. Meeting participants on the front stair of Trolleholm castle Back row, from left: Maria Christensson, Christine Ekdahl-Clementsson, Anders Rasmussen, Mitch Glickstein, Sten Grillner, Mahdi Ghazei, Bror Alstermark, Alan Gibson, Masanobu Kano, Pontus Geborek, Hans Hultborn. Middle row: Benoni Edin, Boris Barbour (sitting), Riccardo Zucca, Martin Garwicz, Carl-Fredrik Ekerot, Jan Voogd, Tim Ebner, Richard Apps, John Rawson, Anton Spanne. Front row (sitting): Fredrik Bentgsson, Chris de Zeeuw, Henrik Jorntell, Germund Hesslow, Fredrik Johansson, Paul Dean, Elzbieta Jankowska, Gert Andersson, Per Kohler ¨ ¨ (standing), Martin Nilsson (standing in front). Missing from the picture: Nadia Cerminara. C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
DOI: 10.1113/jphysiol.2013.265603
5422 detailed series of studies on the spinal and motor information processed by the cells of the lateral reticular nucleus, an important source of mossy fibres to the cerebellum (Clendenin et al. 1974a,b,c; Ekerot, 1990a,b,c). This issue features one original paper and five reviews focused on the analysis of neural circuits using in vivo neurophysiological techniques and informed by the discussions during the symposium. The papers deal with central issues of motor control, ranging from neural mechanisms of action selection triggering motor programmes to the effects of the issued motor commands and the resulting sensory feedback on the circuitry in the cerebellum and in the spinal cord. The first paper describes at a detailed level how the basal ganglia operates in recruiting specific motor centres for eliciting specific motor behaviours (Grillner et al. 2013). It argues that the basic circuitry of the basal ganglia is phylogenetically highly conserved, as are its efferent connections to the brainstem motor centres responsible for different patterns of behaviour, such as eye and locomotor movements, posture and feeding. It describes how the motor centres of the brainstem and neocortex at rest are tonically inhibited by the output of the basal ganglia and that there are various mechanisms within the basal ganglia to release motor programmes from inhibition. Motor centres in the brainstem and neocortex have massive descending pathways that elicit movements via the circuitry in the spinal cord. A large proportion of these descending fibres impinge on different types of spinal interneurons, which integrate the descending motor command with local sensory feedback obtained as the movement progresses. Spinal interneurons in turn mediate the integrated sensorimotor command to alpha-motor neurons and also to the neurons of the spinocerebellar and spinoreticulocerebellar systems. These three major pathways, the dorsal spinocerebellar tract (DSCT), the ventral spinocerebellar tract (VSCT) and the spinoreticulocerebellar (SRCT) pathway are considered at a detailed and functional level in three separate papers. The paper of Stecina et al. (2013) is about the DSCT. Based on recent findings made by this group, they argue that the functional differences between the DSCT and the VSCT may be less pronounced than is commonly thought.
Editorial The paper of Jankowska & Hammar (2013) is about the spinal interneuron inputs to the VSCT. As for the DSCT neurons, a key input to the VSCT neurons is from the spinal interneurons that form part of the local motor circuits of the spinal cord. An important finding that is reviewed is the predominant input from the inhibitory spinal interneurons to the VSCT neurons. The paper of Alstermark & Ekerot (2013) is about the spinoreticulocerebellar system, information from which is transmitted via the lateral reticular nucleus (LRN). It reviews the literature on the information that is integrated by the LRN and proposes a new hypothesis that the function of the LRN may be to use extensive convergence from the different input systems to provide an overview and integration of linked motor components to the cerebellum. The motor command, the spinocerebellar feedback and direct sensory feedback are the major sources of mossy fibre input to the cerebellar systems for forelimb movement control. The information coveyed by some of the mossy fibres, and how it can be used in cerebellar function is discussed in the paper by Dean et al. (2013). This paper takes its origin in the detailed characterization of the neural circuits in the forelimb area of the cerebellar C3 zone and explores how available evidence for these systems can be fitted into an adaptive filter interpretation of cerebellar function under the specific setting of safe limb control. Critical for all theories of cerebellar function in control and learning is the as-yet-unresolved issue of what is signalled by the climbing fibre system. The paper by Horn et al. (2013) provides new data on the role of the climbing fibres by evaluating the behavioural effects of small lesions in specific regions of the inferior olive. The behavioural deficits obtained were generally profound, illustrating the importance of the cerebellum in motor control. The specific deficit obtained was highly dependent on the region of the inferior olive that was targeted and ranged from reach-to-grasp, locomotion, posture and eye movement deficits. The findings are in general agreement with previous ideas that the cerebellum is composed of multiple, functionally distinct compartments, but the paper provides a level of detail in this analysis that has not previously been achieved. All in all, this collection of papers spans many central aspects of neural movement
J Physiol 591.22
control, with emphasis on the spinal cord and the cerebellum. References Alstermark B & Carl-Fredrik Ekerot C-F (2013). The lateral reticular nucleus: a precerebellar centre providing the cerebellum with overview and integration of motor functions at systems level. A new hypothesis. J Physiol 591, 5453–5458. Clendenin M, Ekerot CF & Oscarsson O (1974a). The lateral reticular nucleus in the cat. III. Organization of component activated from ipsilateral forelimb tract. Exp Brain Res 21, 501–513. Clendenin M, Ekerot CF, Oscarsson O & Rosen I (1974b). The lateral reticular nucleus in the cat. I. Mossy fibre distribution in cerebellar cortex. Exp Brain Res 21, 473–486. Clendenin M, Ekerot CF, Oscarsson O & Rosen I (1974c). The lateral reticular nucleus in the cat. II. Organization of component activated from bilateral ventral flexor reflex tract (bVFRT). Exp Brain Res 21, 487–500. Dean P, Anderson S, Porrill J & J¨orntell H (2013). An adaptive filter model of cerebellar zone C3 as a basis for safe limb control? J Physiol 591, 5459–5474. Ekerot CF (1990a). The lateral reticular nucleus in the cat. VI. Excitatory and inhibitory afferent paths. Exp Brain Res 79, 109–119. Ekerot CF (1990b). The lateral reticular nucleus in the cat. VII. Excitatory and inhibitory projection from the ipsilateral forelimb tract (iF tract). Exp Brain Res 79, 120–128. Ekerot CF (1990c). The lateral reticular nucleus in the cat. VIII. Excitatory and inhibitory projection from the bilateral ventral flexor reflex tract (bVFRT). Exp Brain Res 79, 129–137. Ekerot CF, Garwicz M & Schouenborg J (1991). Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J Physiol 441, 257–274. Ekerot CF & Jorntell H (2001). Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 13, 1303–1310. Ekerot CF, Jorntell H & Garwicz M (1995). Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Exp Brain Res 106, 365–376. Ekerot CF & Kano M (1985). Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res 342, 357–360. Ekerot CF & Kano M (1989). Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci Res 6, 264–268.
C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
J Physiol 591.22
Ekerot CF & Larson B (1973). Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. Brain Res 64, 446–450. Ekerot CF & Larson B (1980). Termination in overlapping sagittal zones in cerebellar anterior lobe of mossy and climbing fibre paths activated from dorsal funiculus. Exp Brain Res 38, 163–172. Garwicz M & Ekerot CF (1994). Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol 474, 245–260.
Editorial Garwicz M, J¨orntell H & Ekerot CF (1998). Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone. J Physiol 512, 277–293. Grillner S, Robertson B & Stephenson-Jones M (2013). The evolutionary origin of the vertebrate basal ganglia and its role in action selection. J Physiol 591, 5425–5431. Horn KM, Deep A & Gibson AR (2013). Progressive limb ataxia following inferior olive lesions. J Physiol 591, 5475–5489.
C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
5423 Jankowska E & Hammar I (2013). Interactions between spinal interneurons and ventral spinocerebellar tract neurons. J Physiol 591, 5445–5451. J¨orntell H & Ekerot CF (2002). Reciprocal bidirectional plasticity of parallel fibre receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34, 797–806. Stecina K, Fedirchuk B and Hultborn H (2013). Information to cerebellum on spinal motor networks mediated by the dorsal spinocerebellar tract. J Physiol 591, 5433–5443.
J Physiol 591.22 (2013) pp 5421–5423
Neural circuits in movement control Henrik J¨orntell Neural Basis for Sensorimotor Control, Department of Experimental Medical Science, Lund University, Lund, Sweden Email: [email protected]
A symposium on neural circuits in movement control took place at Trolleholm Castle near Lund on May 27–28, 2011 (Fig. 1). The meeting was a celebration of the
lifetime achievements of Carl-Fredrik Ekerot, who is now retired. The meeting drew together participants from many different disciplines of motor systems neuroscience, but with a focus on the cerebellum and the spinocerebellar systems, which was the main field of interest of Carl-Fredrik Ekerot. Ekerot pioneered the field of climbing fibre microzones in the forelimb area of the C3 zone (Ekerot & Larson, 1980; Ekerot et al. 1991) and the role of the microzones as a functional unit in the cerebellar cortex and in the cerebellar nuclei (Garwicz & Ekerot, 1994;
Ekerot et al. 1995). He provided early evidence of the congruence between mossy fibre and climbing fibre inputs in the cerebellar cortex (Ekerot & Larson, 1973, 1980; Garwicz et al. 1998), made important contributions to early work on cerebellar plasticity research centred on the classical climbing fibre-dependent LTD of parallel fibre synapses on Purkinje cells (Ekerot & Kano, 1985, 1989), later discovering several new forms of plasticity between the parallel fibres and the interneurons and Purkinje cells (Ekerot & Jorntell, 2001; Jorntell & Ekerot, 2002), and made a unique and
The Journal of Physiology
Neuroscience
EDITORIAL
Figure 1. Meeting participants on the front stair of Trolleholm castle Back row, from left: Maria Christensson, Christine Ekdahl-Clementsson, Anders Rasmussen, Mitch Glickstein, Sten Grillner, Mahdi Ghazei, Bror Alstermark, Alan Gibson, Masanobu Kano, Pontus Geborek, Hans Hultborn. Middle row: Benoni Edin, Boris Barbour (sitting), Riccardo Zucca, Martin Garwicz, Carl-Fredrik Ekerot, Jan Voogd, Tim Ebner, Richard Apps, John Rawson, Anton Spanne. Front row (sitting): Fredrik Bentgsson, Chris de Zeeuw, Henrik Jorntell, Germund Hesslow, Fredrik Johansson, Paul Dean, Elzbieta Jankowska, Gert Andersson, Per Kohler ¨ ¨ (standing), Martin Nilsson (standing in front). Missing from the picture: Nadia Cerminara. C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
DOI: 10.1113/jphysiol.2013.265603
5422 detailed series of studies on the spinal and motor information processed by the cells of the lateral reticular nucleus, an important source of mossy fibres to the cerebellum (Clendenin et al. 1974a,b,c; Ekerot, 1990a,b,c). This issue features one original paper and five reviews focused on the analysis of neural circuits using in vivo neurophysiological techniques and informed by the discussions during the symposium. The papers deal with central issues of motor control, ranging from neural mechanisms of action selection triggering motor programmes to the effects of the issued motor commands and the resulting sensory feedback on the circuitry in the cerebellum and in the spinal cord. The first paper describes at a detailed level how the basal ganglia operates in recruiting specific motor centres for eliciting specific motor behaviours (Grillner et al. 2013). It argues that the basic circuitry of the basal ganglia is phylogenetically highly conserved, as are its efferent connections to the brainstem motor centres responsible for different patterns of behaviour, such as eye and locomotor movements, posture and feeding. It describes how the motor centres of the brainstem and neocortex at rest are tonically inhibited by the output of the basal ganglia and that there are various mechanisms within the basal ganglia to release motor programmes from inhibition. Motor centres in the brainstem and neocortex have massive descending pathways that elicit movements via the circuitry in the spinal cord. A large proportion of these descending fibres impinge on different types of spinal interneurons, which integrate the descending motor command with local sensory feedback obtained as the movement progresses. Spinal interneurons in turn mediate the integrated sensorimotor command to alpha-motor neurons and also to the neurons of the spinocerebellar and spinoreticulocerebellar systems. These three major pathways, the dorsal spinocerebellar tract (DSCT), the ventral spinocerebellar tract (VSCT) and the spinoreticulocerebellar (SRCT) pathway are considered at a detailed and functional level in three separate papers. The paper of Stecina et al. (2013) is about the DSCT. Based on recent findings made by this group, they argue that the functional differences between the DSCT and the VSCT may be less pronounced than is commonly thought.
Editorial The paper of Jankowska & Hammar (2013) is about the spinal interneuron inputs to the VSCT. As for the DSCT neurons, a key input to the VSCT neurons is from the spinal interneurons that form part of the local motor circuits of the spinal cord. An important finding that is reviewed is the predominant input from the inhibitory spinal interneurons to the VSCT neurons. The paper of Alstermark & Ekerot (2013) is about the spinoreticulocerebellar system, information from which is transmitted via the lateral reticular nucleus (LRN). It reviews the literature on the information that is integrated by the LRN and proposes a new hypothesis that the function of the LRN may be to use extensive convergence from the different input systems to provide an overview and integration of linked motor components to the cerebellum. The motor command, the spinocerebellar feedback and direct sensory feedback are the major sources of mossy fibre input to the cerebellar systems for forelimb movement control. The information coveyed by some of the mossy fibres, and how it can be used in cerebellar function is discussed in the paper by Dean et al. (2013). This paper takes its origin in the detailed characterization of the neural circuits in the forelimb area of the cerebellar C3 zone and explores how available evidence for these systems can be fitted into an adaptive filter interpretation of cerebellar function under the specific setting of safe limb control. Critical for all theories of cerebellar function in control and learning is the as-yet-unresolved issue of what is signalled by the climbing fibre system. The paper by Horn et al. (2013) provides new data on the role of the climbing fibres by evaluating the behavioural effects of small lesions in specific regions of the inferior olive. The behavioural deficits obtained were generally profound, illustrating the importance of the cerebellum in motor control. The specific deficit obtained was highly dependent on the region of the inferior olive that was targeted and ranged from reach-to-grasp, locomotion, posture and eye movement deficits. The findings are in general agreement with previous ideas that the cerebellum is composed of multiple, functionally distinct compartments, but the paper provides a level of detail in this analysis that has not previously been achieved. All in all, this collection of papers spans many central aspects of neural movement
J Physiol 591.22
control, with emphasis on the spinal cord and the cerebellum. References Alstermark B & Carl-Fredrik Ekerot C-F (2013). The lateral reticular nucleus: a precerebellar centre providing the cerebellum with overview and integration of motor functions at systems level. A new hypothesis. J Physiol 591, 5453–5458. Clendenin M, Ekerot CF & Oscarsson O (1974a). The lateral reticular nucleus in the cat. III. Organization of component activated from ipsilateral forelimb tract. Exp Brain Res 21, 501–513. Clendenin M, Ekerot CF, Oscarsson O & Rosen I (1974b). The lateral reticular nucleus in the cat. I. Mossy fibre distribution in cerebellar cortex. Exp Brain Res 21, 473–486. Clendenin M, Ekerot CF, Oscarsson O & Rosen I (1974c). The lateral reticular nucleus in the cat. II. Organization of component activated from bilateral ventral flexor reflex tract (bVFRT). Exp Brain Res 21, 487–500. Dean P, Anderson S, Porrill J & J¨orntell H (2013). An adaptive filter model of cerebellar zone C3 as a basis for safe limb control? J Physiol 591, 5459–5474. Ekerot CF (1990a). The lateral reticular nucleus in the cat. VI. Excitatory and inhibitory afferent paths. Exp Brain Res 79, 109–119. Ekerot CF (1990b). The lateral reticular nucleus in the cat. VII. Excitatory and inhibitory projection from the ipsilateral forelimb tract (iF tract). Exp Brain Res 79, 120–128. Ekerot CF (1990c). The lateral reticular nucleus in the cat. VIII. Excitatory and inhibitory projection from the bilateral ventral flexor reflex tract (bVFRT). Exp Brain Res 79, 129–137. Ekerot CF, Garwicz M & Schouenborg J (1991). Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J Physiol 441, 257–274. Ekerot CF & Jorntell H (2001). Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 13, 1303–1310. Ekerot CF, Jorntell H & Garwicz M (1995). Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Exp Brain Res 106, 365–376. Ekerot CF & Kano M (1985). Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res 342, 357–360. Ekerot CF & Kano M (1989). Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci Res 6, 264–268.
C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
J Physiol 591.22
Ekerot CF & Larson B (1973). Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. Brain Res 64, 446–450. Ekerot CF & Larson B (1980). Termination in overlapping sagittal zones in cerebellar anterior lobe of mossy and climbing fibre paths activated from dorsal funiculus. Exp Brain Res 38, 163–172. Garwicz M & Ekerot CF (1994). Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat. J Physiol 474, 245–260.
Editorial Garwicz M, J¨orntell H & Ekerot CF (1998). Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone. J Physiol 512, 277–293. Grillner S, Robertson B & Stephenson-Jones M (2013). The evolutionary origin of the vertebrate basal ganglia and its role in action selection. J Physiol 591, 5425–5431. Horn KM, Deep A & Gibson AR (2013). Progressive limb ataxia following inferior olive lesions. J Physiol 591, 5475–5489.
C 2013 The Authors. The Journal of Physiology C 2013 The Physiological Society
5423 Jankowska E & Hammar I (2013). Interactions between spinal interneurons and ventral spinocerebellar tract neurons. J Physiol 591, 5445–5451. J¨orntell H & Ekerot CF (2002). Reciprocal bidirectional plasticity of parallel fibre receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34, 797–806. Stecina K, Fedirchuk B and Hultborn H (2013). Information to cerebellum on spinal motor networks mediated by the dorsal spinocerebellar tract. J Physiol 591, 5433–5443.
