Spinal Mechanisms
Bizzi, E., M. C. Tresch, P. Saltiel, and A. d'Avella. "New Perspectives on Spinal Motor Systems." Nature Reviews/Neuroscience 1 (2000): 101-108.
PubMed abstract: The production and control of complex motor functions are usually attributed to central brain structures such as cortex, basal ganglia and cerebellum. In traditional schemes the spinal cord is assigned a subservient function during the production of movement, playing a predominantly passive role by relaying the commands dictated to it by supraspinal systems. This review challenges this idea by presenting evidence that the spinal motor system is an active participant in several aspects of the production of movement, contributing to functions normally ascribed to 'higher' brain regions.
Mussa-Ivaldi, F. A., and E. Bizzi. "Motor Learning Through the Combination of Primitives." Philosophical Transactions of the Royal Society Lond.: Biological Sciences 355 (2000): 1755-1769.
PubMed abstract: In this paper we discuss a new perspective on how the central nervous system (CNS) represents and solves some of the most fundamental computational problems of motor control. In particular, we consider the task of transforming a planned limb movement into an adequate set of motor commands. To carry out this task the CNS must solve a complex inverse dynamic problem. This problem involves the transformation from a desired motion to the forces that are needed to drive the limb. The inverse dynamic problem is a hard computational challenge because of the need to coordinate multiple limb segments and because of the continuous changes in the mechanical properties of the limbs and of the environment with which they come in contact. A number of studies of motor learning have provided support for the idea that the CNS creates, updates and exploits internal representations of limb dynamics in order to deal with the complexity of inverse dynamics. Here we discuss how such internal representations are likely to be built by combining the modular primitives in the spinal cord as well as other building blocks found in higher brain structures. Experimental studies on spinalized frogs and rats have led to the conclusion that the premotor circuits within the spinal cord are organized into a set of discrete modules. Each module, when activated, induces a specific force field and the simultaneous activation of multiple modules leads to the vectorial combination of the corresponding fields. We regard these force fields as computational primitives that are used by the CNS for generating a rich grammar of motor behaviours.
Kargo, William J., and Simon F. Giszter. "Rapid Correction of Aimed Movements by Summation of Force-Field Primitives." J. Neurosci. 20 (2000): 409-426.
PubMed abstract: Spinal circuits form building blocks for movement construction. In the frog, such building blocks have been described as isometric force fields. Microstimulation studies showed that individual force fields can be combined by vector summation. Summation and scaling of a few force-field types can, in theory, produce a large range of dynamic force-field structures associated with limb behaviors. We tested for the first time whether force-field summation underlies the construction of real limb behavior in the frog. We examined the organization of correction responses that circumvent path obstacles during hindlimb wiping trajectories. Correction responses were triggered on-line during wiping by cutaneous feedback signaling obstacle collision. The correction response activated a force field that summed with an ongoing sequence of force fields activated during wiping. Both impact force and time of impact within the wiping motor pattern scaled the evoked correction response amplitude. However, the duration of the correction response was constant and similar to the duration of other muscles activated in different phases of wiping. Thus, our results confirm that both force-field summation and scaling occur during real limb behavior, that force fields represent fixed-timing motor elements, and that these motor elements are combined in chains and in combination contingent on the interaction of feedback and central motor programs.
Tresch, Mathew C., Philippe Saltiel, and Emilio Bizzi. "The Construction of Movement by the Spinal Cord." Nature Neuroscience 2 (1999): 162-167.
PubMed abstract: We used a computational analysis to identify the basic elements with which the vertebrate spinal cord constructs one complex behavior. This analysis extracted a small set of muscle synergies from the range of muscle activations generated by cutaneous stimulation of the frog hindlimb. The flexible combination of these synergies was able to account for the large number of different motor patterns produced by different animals. These results therefore demonstrate one strategy used by the vertebrate nervous system to produce movement in a computationally simple manner.
PubMed abstract: 1. Although reaching movements are characterized by hand paths that tend to follow roughly straight lines in Cartesian space, a fundamental issue is whether this reflects constraints associated with perception or movement production. 2. To address this issue, we examined two-joint planar reaching movements in which we manipulated the mapping between actual and visually perceived motion. In particular, we used a nonlinear transformation such that straight line hand paths in Cartesian space would result in curved paths in perceived space and vice versa. 3. Under these conditions, subjects learned to make straight line paths in perceived space even though the paths of the hand in Cartesian space were markedly curved. In contrast, when the motion was perceived in Cartesian space (i.e., in the absence of a nonlinear distortion), straight line hand paths were observed. 4. These findings suggest that visually guided reaching movements are planned in a perceptual frame of reference. Reaching movements in the horizontal plane are adapted so as to produce straight lines in visually perceived space.
Hiebert, G. W., and K. G. Pearson. "Contribution of Sensory Feedback to the Generation of Extensor Activity During Walking in the Decerebrate Cat." J. Neurophysiol 81 (1999): 758-770. (0022-3077/99 The American Physiological Society.)
PubMed abstract: In this investigation we have estimated the afferent contribution to the generation of activity in the knee and ankle extensor muscles during walking in decerebrate cats by loading and unloading extensor muscles, and by unilateral deafferentation of a hind leg. The total contribution of afferent feedback to extensor burst generation was estimated by allowing one hind leg to step into a hole in the treadmill belt on which the animal was walking. In the absence of ground support the level of activity in knee and ankle extensor muscles was reduced to approximately 70% of normal. Activity in the ankle extensors could be restored during the "foot-in-hole" trials by selectively resisting extension at the ankle. Thus feedback from proprioceptors in the ankle extensor muscles probably makes a large contribution to burst generation in these muscles during weight-bearing steps. Similarly, feedback from proprioceptors in knee extensor appears to contribute substantially to the activation of knee extensor muscles because unloading and loading these muscles, by lifting and dropping the hindquarters, strongly reduced and increased, respectively, the level of activity in the knee extensors. This conclusion was supported by the finding that partial deafferentation of one hind leg by transection of the L4-L6 dorsal roots reduced the level of activity in the knee extensors by approximately 50%, but did not noticeably influence the activity in ankle extensor muscles. However, extending the deafferentation to include the L7-S2 dorsal roots decreased the ankle extensor activity. We conclude that afferent feedback contributes to more than one-half of the input to knee and ankle extensor motoneurons during the stance phase of walking in decerebrate cats. The continuous contribution of afferent feedback to the generation of extensor activity could function to automatically adjust the intensity of activity to meet external demands.
Kandel, Schwartz, and Jessell. "Locomotion."
Kjaerulff, O., and O. Kiehn. "Distribution of Networks Generating and Coordinating Locomotor Activity in the Neonatal Rat Spinal Cord in Vitro: A Lesion Study." The Journal of Neuroscience 16, 18 (1996): 5777-5794.
PubMed abstract: The isolated spinal cord of the newborn rat contains networks that are able to create a patterned motor output resembling normal locomotor movements. In this study, we sought to localize the regions of primary importance for rhythm and pattern generation using specific mechanical lesions. We used ventral root recordings to monitor neuronal activity and tested the ability of various isolated parts of the caudal thoraciclumbar cord to generate rhythmic bursting in a combination of 5-HT and NMDA. In addition, pathways mediating left/right and rostrocaudal burst alternation were localized. We found that the isolated ventral third of the spinal cord can generate normally coordinated rhythmic activity, whereas lateral fragments resulting from sagittal sections showed little or no rhythmogenic capability compared with intact control preparations. The ability to generate fast and regular rhythmic activity decreased in the caudal direction, but the rhythm-generating network was found to be distributed over the entire lumbar region and to extend into the caudal thoracic region. The pathways mediating left/ right alternation exist primarily in the ventral commissure. As with the rhythmogenic ability, these pathways were distributed along the lumbar enlargement. Both lateral and ventral funiculi were sufficient to coordinate activity in the rostral and caudal regions. We conclude that the networks organizing locomotor-related activity in the spinal cord of the newborn rat are distributed.
Vallbo, A. B., and J. Wessberg. "Organization of Motor Output in Slow Finger Movements in Man." Journal of Physiology 469 (1993): 673-691.
PubMed abstract: 1. Slow finger movements were analysed in normal human subjects with regard to kinematics and EMG activity of the long finger muscles. Surface EMG from the finger extensor and flexor muscles on the forearm was recorded along with angular position and angular velocity during voluntary ramp movements at single metacarpophalangeal joints. Angular acceleration was computed from the velocity record. 2. It was found that movements were not smooth but characterized by steps or discontinuities, often recurring at intervals of 100-125 ms, yielding velocity and acceleration profiles dominated by 8-10 Hz cycles. The discontinuities were manifest from the very first trial and thus not dependent on training. Their amplitude and amount varied between subjects but were relatively stable for the individual subject. 3. The 8-10 Hz cycles were seen with voluntary ramp movements of widely varying velocities, higher velocities being associated with larger steps recurring with the same repetition rate as the small steps of slow voluntary ramps. Maximal step amplitude observed was more than one order of magnitude larger than physiological tremor. 4. The individual 8-10 Hz cycle was asymmetrical in that decelerations usually reached higher peaks than the preceding acceleration, suggesting that the antagonist contributed with a braking action. Moreover, in very slow voluntary ramps, the movement cycles were often interspaced by periods of zero velocity, providing a highly non-sinusoidal velocity profile. 5. The EMG of the agonist and the antagonist muscles was modulated in close relation to the accelerations and decelerations respectively of the individual movement cycle. These modulations were present in both extensor and flexor muscles, although they were more consistent and usually more prominent in the former. 6. The findings indicate that a feature of slow finger movements was an 8-10 Hz periodic output to the muscular system, suggesting that slow finger movements are implemented by a series of biphasic force pulses, involving not only the shortening agonist muscle propelling the movement, but the antagonist muscle as well whose activity increased shortly after the agonist and contributed to a sharp deceleration of the individual step of movement. 7. It is proposed, as a hypothesis, that this biphasic motor output may reflect a similar organization of the descending motor command for slow finger movements. Hence, this command would include a series of biphasic pulses, concatenated at a rate of 8-10 per second and a pulse-height regulator capable of setting the size of the pulse and thus the overall speed of the movement.
PubMed abstract: This is the third in a series of studies of the neural representation of tactile spatial form in somatosensory cortical area 3b of the alert monkey. We previously studied the spatial structure of >350 fingerpad receptive fields (RFs) with random-dot patterns scanned in one direction () and at varying velocities (). Those studies showed that area 3b RFs have a wide range of spatial structures that are virtually unaffected by changes in scanning velocity. In this study, 62 area 3b neurons were studied with three to eight scanning directions (58 with four or more directions). The data from all three studies are described accurately by an RF model with three components: (1) a single, central excitatory region of short duration, (2) one or more inhibitory regions, also of short duration, that are adjacent to and nearly synchronous with the excitation, and (3) a region of inhibition that overlaps the excitation partially or totally and is temporally delayed with respect to the first two components. The mean correlation between the observed RFs and the RFs predicted by this three-component model was 0.81. The three-component RFs also predicted orientation sensitivity and preferred orientation to a scanned bar accurately. The orientation sensitivity was determined most strongly by the intensity of the coincident RF inhibition in relation to the excitation. Both orientation sensitivity and this ratio were stronger in the supragranular and infragranular layers than in layer IV.
DiCarlo, J. J., K. O. Johnson, and S. S. Hsiao. "Structure of Receptive Fields in Area 3B of Primary Somatosensory Cortex in the Alert Monkey." J. Neurosci. 18, 7 (1998): 2626-2645.
PubMed abstract: We investigated the two-dimensional structure of area 3b neuronal receptive fields (RFs) in three alert monkeys. Three hundred thirty neurons with RFs on the distal fingerpads were studied with scanned, random dot stimuli. Each neuron was stimulated continuously for 14 min, yielding 20,000 response data points. Excitatory and inhibitory components of each RF were determined with a modified linear regression algorithm. Analyses assessing goodness-of-fit, repeatability, and generality of the RFs were developed. Two hundred forty-seven neurons yielded highly repeatable RF estimates, and most RFs accounted for a large fraction of the explainable response of each neuron. Although the area 3b RF structures appeared to be continuously distributed, certain structural generalities were apparent. Most RFs (94%) contained a single, central region of excitation and one or more regions of inhibition located on one, two, three, or all four sides of the excitatory center. The shape, area, and strength of excitatory and inhibitory RF regions ranged widely. Half the RFs contained almost evenly balanced excitation and inhibition. The findings indicate that area 3b neurons act as local spatiotemporal filters that are maximally excited by the presence of particular stimulus features. We believe that form and texture perception are based on high-level representations and that area 3b is an intermediate stage in the processes leading to these representations. Two possibilities are considered: (1) that these high-level representations are basically somatotopic and that area 3b neurons amplify some features and suppress others, or (2) that these representations are highly transformed and that area 3b effects a step in the transformation.
Florence, S. L., N. Jain, M. W. Pospichal, P. D. Beck, D. L. Sly, and J. H. Kaas. "Central Reorganization of Sensory Pathways Following Peripheral Nerve Regeneration in Fetal Monkeys." Nature 381 (1996): 69-71.
PubMed abstract: Transection of a sensory nerve in adults results in profound abnormalities in sensory perception, even if the severed nerve is surgically repaired to facilitate accurate nerve regeneration. In marked contrast, fewer perceptual errors follow nerve transection and surgical repair in children. The basis for this superior recovery in children was unknown. Here we show that there is little or no topographic order in the median nerve to the hand after median nerve section and surgical repair in immature macaque monkeys. Remarkably, however, in the same animals the representation of the reinnervated hand in primary somatosensory cortex area (area 3b) is quite orderly. This indicates that there are mechanisms in the developing brain that can create cortical topography, despite disordered sensory inputs. Presumably the superior recovery of perceptual abilities after peripheral nerve transection in children depends on this restoration of somatotopy in the central sensory maps.
Johnson, K. O. "Neural Coding." Neuron 26 (2000): 563-566.
Kaas, J. H. "Plasticity of Sensory and Motor Maps in Adult Mammals." Annu. Rev. of Neurosci. 14 (1991): 137-67.
Moore, C. I., S. B. Nelson, and M. Sur. "Dynamics of Neuronal Processing in Rat Somatosensory Cortex." Trends in Neurosciences 22 (1999): 513-520.
PubMed abstract: Recently, the study of sensory cortex has focused on the context-dependent evolution of receptive fields and cortical maps over millisecond to second time-scales. This article reviews advances in our understanding of these processes in the rat primary somatosensory cortex (SI). Subthreshold input to individual rat SI neurons is extensive, spanning several vibrissae from the center of the receptive field, and arrives within 25 ms of vibrissa deflection. These large subthreshold receptive fields provide a broad substrate for rapid excitatory and inhibitory multi-vibrissa interactions. The 'whisking' behavior, an approximately 8 Hz ellipsoid movement of the vibrissae, introduces a context-dependent change in the pattern of vibrissa movement during tactile exploration. Stimulation of vibrissae over this frequency range modulates the pattern of activity in thalamic and cortical neurons, and, at the level of the cortical map, focuses the extent of the vibrissa representation relative to lower frequency stimulation (1 Hz). These findings suggest that one function of whisking is to reset cortical organization to improve tactile discrimination. Recent discoveries in primary visual cortex (VI) demonstrate parallel non-linearities in center-surround interactions in rat SI and VI, and provide a model for the rapid integration of multi-vibrissa input. The studies discussed in this article suggest that, despite its original conception as a uniquely segregated cortex, rat SI has a wide array of dynamic interactions, and that the study of this region will provide insight into the general mechanisms of cortical dynamics engaged by sensory systems.
Nicolelis, M. A. L., A. A. Ghazanfar, C. R. Stambaugh, L. M. O. Oliveira, M. Laubach, J. K. Chapin, R. J. Nelson, and J. H. Kaas. "Simultaneous Encoding of Tactile Information by Three Primate Cortical Areas." Nature Neuroscience 7 (1998): 621-630.
PubMed abstract: We used simultaneous multi-site neural ensemble recordings to investigate the representation of tactile information in three areas of the primate somatosensory cortex (areas 3b, SII and 2). Small neural ensembles (30-40 neurons) of broadly tuned somatosensory neurons were able to identify correctly the location of a single tactile stimulus on a single trial, almost simultaneously. Furthermore, each of these cortical areas could use different combinations of encoding strategies, such as mean firing rate (areas 3b and 2) or temporal patterns of ensemble firing (area SII), to represent the location of a tactile stimulus. Based on these results, we propose that ensembles of broadly tuned neurons, located in three distinct areas of the primate somatosensory cortex, obtain information about the location of a tactile stimulus almost concurrently.
Racanzone, G. H., M. M. Merzenich, and C. E. Schreiner. "Changes in the Distributed Temporal Response Properties of SI Cortical Neurons Reflect Improvements in Performance on a Temporally Based Tactile Discrimination Task." J. Neurophys. 67 (1992): 1071-1091.
PubMed abstract: 1. Temporal response characteristics of neurons were sampled in fine spatial grain throughout the hand representations in cortical areas 3a and 3b in adult owl monkeys. These monkeys had been trained to detect small differences in tactile stimulus frequencies in the range of 20-30 Hz. Stimuli were presented to an invariant, restricted spot on a single digit. 2. The absolute numbers of cortical locations and the cortical area over which neurons showed entrained frequency-following responses to behaviorally important stimuli were significantly greater when stimulation was applied to the trained skin, as compared with stimulation on an adjacent control digit, or at corresponding skin sites in passively stimulated control animals. 3. Representational maps defined with sinusoidal stimuli were not identical to maps defined with just-visible tapping stimuli. Receptive-field/frequency-following response site mismatches were recorded in every trained monkey. Mismatches were less frequently recorded in the representations of control skin surfaces. 4. At cortical locations with entrained responses, neither the absolute firing rates of neurons nor the degree of the entrainment of the response were correlated with behavioral discrimination performance. 5. All area 3b cortical locations with entrained responses evoked by stimulation at trained or untrained skin sites were combined to create population peristimulus time and cycle histograms. In all cases, stimulation of the trained skin resulted in 1) larger-amplitude responses, 2) peak responses earlier in the stimulus cycle, and 3) temporally sharper responses, than did stimulation applied to control skin sites. 6. The sharpening of the response of cortical area 3b neurons relative to the period of the stimulus could be accounted for by a large subpopulation of neurons that had highly coherent responses. 7. Analysis of cycle histograms for area 3b neuron responses revealed that the decreased variance in the representation of each stimulus cycle could account for behaviorally measured frequency discrimination performance. A strong correlation between these temporal response distributions and the discriminative performances for stimuli applied at all studied skin surfaces was even stronger (r = 0.98) if only the rising phases of cycle histogram were considered in the analysis. 8. The responses of neurons in area 3a could not account for measured differences in frequency discrimination performance. 9. These representational changes did not occur in monkeys that were stimulated on the same schedule but were performing an auditory discrimination task during skin stimulation. 10. It is concluded that by behaviorally training adult owl monkeys to discriminate the temporal features of a tactile stimulus, distributed spatial and temporal response properties of cortical neurons are altered.
Romo, R., A. Hernandez, A. Zainos, and E. Salinas. "Somatosensory Discrimination Based on Cortical Microstimulation." Nature 392 (1998): 387-390.
PubMed abstract: The sensation of flutter is produced when mechanical vibrations in the range of 5-50Hz are applied to the skin. A flutter stimulus activates neurons in the primary somatosensory cortex (S1) that somatotopically map to the site of stimulation. A subset of these neurons-those with quickly adapting properties, associated with Meissner's corpuscles-are strongly entrained by periodic flutter vibrations, firing with a probability that oscillates at the input frequency. Hence, quickly adapting neurons provide a dynamic representation of such flutter stimuli. However, are these neurons directly involved in the perception of flutter? Here we investigate this in monkeys trained to discriminate the difference in frequency between two flutter stimuli delivered sequentially on the fingertips. Microelectrodes were inserted into area 3b of S1 and the second stimulus was substituted with a train of injected current pulses. Animals reliably indicated whether the frequency of the second (electrical) signal was higher or lower than that of the first (mechanical) signal, even though both frequencies changed from trial to trial. Almost identical results were obtained with periodic and aperiodic stimuli of equal average frequencies. Thus, the quickly adapting neurons in area 3b activate the circuit leading to the perception of flutter. Furthermore, as far as can be psychophysically quantified during discrimination, the neural code underlying the sensation of flutter can be finely manipulated, to the extent that the behavioural responses produced by natural and artificial stimuli are indistinguishable.
Romo, R., and E. Salinas. "Touch and Go: Decision-Making Mechanisms in Somatosensation." Annu. Rev. Neurosci. 24 (2001): 107-37.
PubMed abstract: A complex sequence of neural events unfolds between sensory receptor activation and motor activity. To understand the underlying decision-making mechanisms linking somatic sensation and action, we ask what components of the neural activity evoked by a stimulus are directly related to psychophysical performance, and how are they related. We find that single-neuron responses in primary and secondary somatosensory cortices account for the observed performance of monkeys in vibrotactile discrimination tasks, and that neuronal and behavioral responses covary in single trials. This sensory activity, which provides input to memory and decision-making mechanisms, is modulated by attention and behavioral context, and microstimulation experiments indicate that it may trigger normal perceptual experiences. Responses recorded in motor areas seem to reflect the output of decision-making operations, which suggests that the ability to make decisions occurs at the sensory-motor interface.
Sheth, B., C. I. Moore, and M. Sur. "Temporal Modulation of Spatial Borders in Rat Barrel Cortex." J.Neurophys. 79 (1998): 464-470.
PubMed abstract: We examined the effects of varying vibrissa stimulation frequency on intrinsic signal and neuronal responses in rat barrel cortex. Optical imaging of intrinsic signals demonstrated that the region of cortex activated by deflection of a single vibrissa at 1 Hz is more diffuse and more widespread than the territory activated at 5 or 10 Hz. With the use of two different paradigms, constant time of stimulation and constant number of vibrissa deflections, we showed that the optically imaged spread of activity is more discrete at higher stimulation frequencies. We combined optical imaging with multiple electrode recording and confirmed that the neuronal response to individual vibrissa stimulation at the optically imaged center of activity is greater than the response away from the imaged center. Consistent with the imaging data, these recordings also showed no response to a second vibrissa deflection at 5 Hz at a peripheral recording site, though there was a significant response to a second vibrissa deflection at 1 Hz at the same peripheral site. These findings demonstrate that vibrissa stimulation at higher frequencies leads to more focused physiological responses in cortex. Thus the spread of activation in rat barrel cortex is modulated in a dynamic fashion by the frequency of vibrissa stimulation.
Steinmetz, P. N., A. Roy, P. J. Fitzgerald, S. S. Hsiao, K. O. Johnson , and E. Niebur. "Attention Modulates Synchronized Neuronal Firing in Primate Somatosensory Cortex." Nature 404 (2000): 187-190.
PubMed abstract: A potentially powerful information processing strategy in the brain is to take advantage of the temporal structure of neuronal spike trains. An increase in synchrony within the neural representation of an object or location increases the efficacy of that neural representation at the next synaptic stage in the brain; thus, increasing synchrony is a candidate for the neural correlate of attentional selection. We investigated the synchronous firing of pairs of neurons in the secondary somatosensory cortex (SII) of three monkeys trained to switch attention between a visual task and a tactile discrimination task. We found that most neuron pairs in SII cortex fired synchronously and, furthermore, that the degree of synchrony was affected by the monkey's attentional state. In the monkey performing the most difficult task, 35% of neuron pairs that fired synchronously changed their degree of synchrony when the monkey switched attention between the tactile and visual tasks. Synchrony increased in 80% and decreased in 20% of neuron pairs affected by attention.
Sur, M. "Somatosensory Cortex. Maps of Time and Space." Nature 378 (1995): 13-14.
Wang, X., M. M. Merzenich, K. Sameshima, and W. M. Jenkins. "Remodeling of Hand Representation in Adult Cortex Determined by Timing of Tactile Stimulation." Nature 378 (1995): 71-75. (With commentary.)
PubMed abstract: The primate somatosensory cortex, which processes tactile stimuli, contains a topographic representation of the signals it receives, but the way in which such maps are maintained is poorly understood. Previous studies of cortical plasticity indicated that changes in cortical representation during learning arise largely as a result of hebbian synaptic change mechanisms. Here we show, using owl monkeys trained to respond to specific stimulus sequence events, that serial application of stimuli to the fingers results in changes to the neuronal response specificity and maps of the hand surfaces in the true primary somatosensory cortical field (S1 area 3b). In this representational remodelling stimuli applied asychronously to the fingers resulted in these fingers being integrated in their representation, whereas fingers to which stimuli were applied asynchronously were segregated in their representation. Ventroposterior thalamus response maps derived in these monkeys were not equivalently reorganized. This representational plasticity appears to be cortical in origin.
PubMed abstract: Learning a motor skill sets in motion neural processes that continue to evolve after practice has ended, a phenomenon known as consolidation. Here we present psychophysical evidence for this, and show that consolidation of a motor skill was disrupted when a second motor task was learned immediately after the first. There was no disruption if four hours elapsed between learning the two motor skills, with consolidation occurring gradually over this period. Previous studies in humans and other primates have found this time-dependent disruption of consolidation only in explicit memory tasks, which rely on brain structures in the medial temporal lobe. Our results indicate that motor memories, which do not depend on the medial temporal lobe, can be transformed by a similar process of consolidation. By extending the phenomenon of consolidation to motor memory, our results indicate that distinct neural systems share similar characteristics when encoding and storing new information.
Gandolfo, F., C. S. R. Li, B. J. Benda, C. P. Schioppa, and E. Bizzi. "Cortical Correlates of Learning in Monkeys Adapting to a New Dynamical Environment." PNAS 97 (2000): 2259-2263.
PubMed abstract: In this paper, we describe the neural changes observed in the primary motor cortex of two monkeys while they learned a new motor skill. The monkeys had to adapt their reaching movements to external forces that interfered with the execution of their arm movements. We found a sizable population of cells that changed their tuning properties during exposure to the force field. These cells took on the properties of neurons that are involved in the control of movement. Furthermore, the cells maintained the acquired activity as the monkey readapted to the no-force condition. Recent imaging studies in humans have reported the effects of motor learning in the primary motor cortex. Our results are consistent with the findings of these studies and provide evidence for single-cell plasticity in the primary motor cortex of primates.
Georgopoulos, A. P., A. B. Schwartz, and R. E. Kettner. "Neuronal Population Coding of Movement Direction." Science 233 (1986): 1416-1419.
PubMed abstract: Although individual neurons in the arm area of the primate motor cortex are only broadly tuned to a particular direction in three-dimensional space, the animal can very precisely control the movement of its arm. The direction of movement was found to be uniquely predicted by the action of a population of motor cortical neurons. When individual cells were represented as vectors that make weighted contributions along the axis of their preferred direction (according to changes in their activity during the movement under consideration) the resulting vector sum of all cell vectors (population vector) was in a direction congruent with the direction of movement. This population vector can be monitored during various tasks, and similar measures in other neuronal populations could be of heuristic value where there is a neural representation of variables with vectorial attributes.
Georgopoulos, A. P., J. F. Kalaska, R. Caminiti, and J. T. Massey. "On the Relations Between the Direction of Two-Dimensional Arm Movements and Cell Discharge in Primate Motor Cortex." J. Neurosci. 2 (1982): 1527-1537.
PubMed abstract: The activity of single cells in the motor cortex was recorded while monkeys made arm movements in eight directions (at 45 degrees intervals) in a two-dimensional apparatus. These movements started from the same point and were of the same amplitude. The activity of 606 cells related to proximal arm movements was examined in the task; 323 of the 606 cells were active in that task and were studied in detail. The frequency of discharge of 241 of the 323 cells (74.6%) varied in an orderly fashion with the direction of movement. Discharge was most intense with movements in a preferred direction and was reduced gradually when movements were made in directions farther and farther away from the preferred one. This resulted in a bell-shaped directional tuning curve. These relations were observed for cell discharge during the reaction time, the movement time, and the period that preceded the earliest changes in the electromyographic activity (approximately 80 msec before movement onset). In about 75% of the 241 directionally tuned cells, the frequency of discharge, D, was a sinusoidal function of the direction of movement, theta: D = b0 + b1 sin theta + b2cos theta, or, in terms of the preferred direction, theta 0: D = b0 + c1cos (theta - theta0), where b0, b1, b2, and c1 are regression coefficients. Preferred directions differed for different cells so that the tuning curves partially overlapped. The orderly variation of cell discharge with the direction of movement and the fact that cells related to only one of the eight directions of movement tested were rarely observed indicate that movements in a particular direction are not subserved by motor cortical cells uniquely related to that movement. It is suggested, instead, that a movement trajectory in a desired direction might be generated by the cooperation of cells with overlapping tuning curves. The nature of this hypothetical population code for movement direction remains to be elucidated.
Grafton, S.T., E. Hazeltine, and R. B. Ibry. "Abstract and Effector-Specific Representations of Motor Sequences Identified with PET." J. Neurosci. 18 (1998): 9420-9428.
PubMed abstract: Positron emission tomography was used to identify neural systems involved in the acquisition and expression of sequential movements produced by different effectors. Subjects were tested on the serial reaction time task under implicit learning conditions. In the initial acquisition phase, subjects responded to the stimuli with keypresses using the four fingers of the right hand. During this phase, the stimuli followed a fixed sequence for one group of subjects (group A) and were randomly selected for another group (group B). In the transfer phase, arm movements were used to press keys on a substantially larger keyboard, and for both groups, the stimuli followed the sequence. Behavioral indices provided clear evidence of learning during the acquisition phase for group A and transfer when switched to the large keyboard. Sequence acquisition was associated with learning-related increases in regional cerebral blood flow (rCBF) in a network of areas in the contralateral left hemisphere, including sensorimotor cortex, supplementary motor area, and rostral inferior parietal cortex. After transfer, activity in inferior parietal cortex remained high, suggesting that this area had encoded the sequence at an abstract level independent of the particular effectors used to perform the task. In contrast, activity in sensorimotor cortex shifted to a more dorsal locus, consistent with motor cortex somatotopy. Thus, activity here was effector-specific. An increase in rCBF was also observed in the cingulate motor area at transfer, suggesting a role linking the abstract sequential representations with the task-relevant effector system. These results highlight a network of areas involved in sequence encoding and retrieval.
Grafton, S.T., J. Salidis, and D. B. Willingham. "Motor Learning of Compatible and Incompatible Visuomotor Maps." J. Cog. Neurosci. 13 (2001): 217-231.
PubMed abstract: Brain imaging studies demonstrate increasing activity in limb motor areas during early motor skill learning, consistent with functional reorganization occurring at the motor output level. Nevertheless, behavioral studies reveal that visually guided skills can also be learned with respect to target location or possibly eye movements. The current experiments examined motor learning under compatible and incompatible perceptual/motor conditions to identify brain areas involved in different perceptual-motor transformations. Subjects tracked a continuously moving target with a joystick-controlled cursor. The target moved in a repeating sequence embedded within random movements to block sequence awareness. Psychophysical studies of behavioral transfer from incompatible (joystick and cursor moving in opposite directions) to compatible tracking established that incompatible learning was occurring with respect to target location. Positron emission tomography (PET) functional imaging of compatible learning identified increasing activity throughout the precentral gyrus, maximal in the arm area. Incompatible learning also led to increasing activity in the precentral gyrus, maximal in the putative frontal eye fields. When the incompatible task was switched to a compatible response and the previously learned sequence was reintroduced, there was an increase in arm motor cortex. The results show that learning-related increases of brain activity are dynamic, with recruitment of multiple motor output areas, contingent on task demands. Visually guided motor sequences can be linked to either oculomotor or arm motor areas. Rather than identifying changes of motor output maps, the data from imaging experiments may better reflect modulation of inputs to multiple motor areas.
Graziano, M. S. A., and C. G. Gross. "Spatial Maps for the Control of Movement." Curr. Opin. Neurobiol. 8 (1998): 195-201.
PubMed abstract: Neurons in the ventral premotor cortex of the monkey encode the locations of visual, tactile, auditory and remembered stimuli. Some of these neurons encode the locations of stimuli with respect to the arm, and may be useful for guiding movements of the arm. Others encode the locations of stimuli with respect to the head, and may be useful for guiding movements of the head. We suggest that a general principle of sensory-motor integration is that the space surrounding the body is represented in body-part-centered coordinates. That is, there are multiple coordinate systems used to guide movement, each one attached to a different part of the body. This and other recent evidence from both monkeys and humans suggest that the formation of spatial maps in the brain and the guidance of limb and body movements do not proceed in separate stages but are closely integrated in both the parietal and frontal lobes.
Kakei, S., D. S. Hoffman, and P. L. Strick. "Muscle and Movement Representations in the Primary Motor Cortex." Science 285 (1999): 2136-2139.
PubMed abstract: What aspects of movement are represented in the primary motor cortex (M1): relatively low-level parameters like muscle force, or more abstract parameters like handpath? To examine this issue, the activity of neurons in M1 was recorded in a monkey trained to perform a task that dissociates three major variables of wrist movement: muscle activity, direction of movement at the wrist joint, and direction of movement in space. A substantial group of neurons in M1 (28 out of 88) displayed changes in activity that were muscle-like. Unexpectedly, an even larger group of neurons in M1 (44 out of 88) displayed changes in activity that were related to the direction of wrist movement in space independent of the pattern of muscle activity that generated the movement. Thus, both "muscles" and "movements" appear to be strongly represented in M1.
Kalaska, J. F., S. H. Scott, P. Cisek, and L. Sergio. "Cortical Control of Reaching Movements." Curr. Opin. Neurobiol. 7 (1997): 849-859.
PubMed abstract: Recent studies provide further support for the hypothesis that spatial representations of limb position, target locations, and potential motor actions are expressed in the neuronal activity in parietal cortex. In contrast, precentral cortical activity more strongly expresses processes involved in the selection and execution of motor actions. As a general conceptual framework, these processes may be interpreted in terms of such formalisms as sensorimotor transformations and 'internal models'.
Kandel, R., J. H. Schwartz, and T. M. Jessell, eds. "Voluntary Movement." In Principles of Neural Science, 4th ed. New York: McGraw-Hill, 2000, pp. 756-781.
Kleim, J. A., S. Barbay, and R. J. Nudo. "Functional Reorganization of the Rat Motor Cortex Following Motor Skill Learning." J. Neurophysiol. 80 (1998): 3321-3325.
PubMed abstract: Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 80: 3321-3325, 1998. Adult rats were allocated to either a skilled or unskilled reaching condition (SRC and URC, respectively). SRC animals were trained for 10 days on a skilled reaching task while URC animals were trained on a simple bar pressing task. After training, microelectrode stimulation was used to derive high resolution maps of the forelimb and hindlimb representations within the motor cortex. In comparison with URC animals, SRC animals exhibited a significant increase in mean area of the wrist and digit representations but a decrease in elbow/shoulder representation within the caudal forelimb area. No between-group differences in areal representation were found in either the hindlimb or rostral forelimb areas. These results demonstrate that motor skill learning is associated with a reorganization of movement representations within the rodent motor cortex.
Li, C. S. R., C. Padoa-Schioppa, and E. Bizzi. "Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field." Neuron 30 (2001): 593-607.
PubMed abstract: The primary motor cortex (M1) is known to control motor performance. Recent findings have also implicated M1 in motor learning, as neurons in this area show learning-related plasticity. In the present study, we analyzed the neuronal activity recorded in M1 in a force field adaptation task. Our goal was to investigate the neuronal reorganization across behavioral epochs (before, during, and after adaptation). Here we report two main findings. First, memory cells were present in two classes. With respect to the changes of preferred direction (Pd), these two classes complemented each other after readaptation. Second, for the entire neuronal population, the shift of Pd matched the shift observed for muscles. These results provide a framework whereby the activity of distinct neuronal subpopulations combines to subserve both functions of motor performance and motor learning.
Muellbacher, W., U. Ziemann, J. Wissel, N. Dang, M. Kofler, S. Facchini, B. Boroojerdi, W. Poewe, and M. Hallett. "Early Consolidation in Human Primary Motor Cortex." Nature 415 (2002): 640-644.
PubMed abstract: Behavioural studies indicate that a newly acquired motor skill is rapidly consolidated from an initially unstable state to a more stable state, whereas neuroimaging studies demonstrate that the brain engages new regions for performance of the task as a result of this consolidation. However, it is not known where a new skill is retained and processed before it is firmly consolidated. Some early aspects of motor skill acquisition involve the primary motor cortex (M1), but the nature of that involvement is unclear. We tested the possibility that the human M1 is essential to early motor consolidation. We monitored changes in elementary motor behaviour while subjects practised fast finger movements that rapidly improved in movement acceleration and muscle force generation. Here we show that low-frequency, repetitive transcranial magnetic stimulation of M1 but not other brain areas specifically disrupted the retention of the behavioural improvement, but did not affect basal motor behaviour, task performance, motor learning by subsequent practice, or recall of the newly acquired motor skill. These findings indicate that the human M1 is specifically engaged during the early stage of motor consolidation.
Rioult-Pedotti, M. S., D. Friedman, G. Hess, and J. P. Donoghue. "Strengthening of Horizontal Cortical Connections Following Skill Learning." Nat. Neurosci. 1 (1998): 230-234.
PubMed abstract: Learning a new motor skill requires an alteration in the spatiotemporal pattern of muscle activation. Motor areas of cerebral neocortex are thought to be involved in this type of learning, possibly by functional reorganization of cortical connections. Here we show that skill learning is accompanied by changes in the strength of connections within adult rat primary motor cortex (M1). Rats were trained for three or five days in a skilled reaching task with one forelimb, after which slices of motor cortex were examined to determine the effect of training on the strength of horizontal intracortical connections in layer II/III. The amplitude of field potentials in the forelimb region contralateral to the trained limb was significantly increased relative to the opposite 'untrained' hemisphere. No differences were seen in the hindlimb region. Moreover, the amount of long-term potentiation (LTP) that could be induced in trained M1 was less than in controls, suggesting that the effect of training was at least partly due to LTP-like mechanisms. These data represent the first direct evidence that plasticity of intracortical connections is associated with learning a new motor skill.
Rioult-Pedotti, M. S., F. Friedman, and J. P. Donoghue. "Learning-Induced LTP in Neocortex." Science 290 (2000): 533-536.
PubMed abstract: The hypothesis that learning occurs through long-term potentiation (LTP)- and long-term depression (LTD)-like mechanisms is widely held but unproven. This hypothesis makes three assumptions: Synapses are modifiable, they modify with learning, and they strengthen through an LTP-like mechanism. We previously established the ability for synaptic modification and a synaptic strengthening with motor skill learning in horizontal connections of the rat motor cortex (MI). Here we investigated whether learning strengthened these connections through LTP. We demonstrated that synapses in the trained MI were near the ceiling of their modification range, compared with the untrained MI, but the range of synaptic modification was not affected by learning. In the trained MI, LTP was markedly reduced and LTD was enhanced. These results are consistent with the use of LTP to strengthen synapses during learning.
Rizzolatti, G., L. Fadiga, V. Gallese, and L. Fogassi. "Premotor Cortex and the Recognition of Motor Actions." Cog. Br. Res. 3 (1996): 131-141.
PubMed abstract: In area F5 of the monkey premotor cortex there are neurons that discharge both when the monkey performs an action and when he observes a similar action made by another monkey or by the experimenter. We report here some of the properties of these 'mirror' neurons and we propose that their activity 'represents' the observed action. We posit, then, that this motor representation is at the basis of the understanding of motor events. Finally, on the basis of some recent data showing that, in man, the observation of motor actions activate the posterior part of inferior frontal gyrus, we suggest that the development of the lateral verbal communication system in man derives from a more ancient communication system based on recognition of hand and face gestures.
Rizzolatti, G., L. Fogassi, and V. Gallese. "Parietal Cortex: From Sight to Action." Curr. Opin. Neurobiol. 7 (1997): 562-567.
PubMed abstract: Recent findings have altered radically our thinking about the functional role of the parietal cortex. According to this view, the parietal lobe consists of a multiplicity of areas with specific connections to the frontal lobe. These areas, together with the frontal areas to which they are connected, mediate distinct sensorimotor transformations related to the control of hand, arm, eye or head movements. Space perception is not unitary, but derives from the joint activity of the fronto-parietal circuits that control actions requiring space computation.
Sanes, J. N., and J. P. Donoghue. "Plasticity and Primary Motor Cortex." Annu. Rev. Neurosci. 23 (2000): 393-415.
PubMed abstract: One fundamental function of primary motor cortex (MI) is to control voluntary movements. Recent evidence suggests that this role emerges from distributed networks rather than discrete representations and that in adult mammals these networks are capable of modification. Neuronal recordings and activation patterns revealed with neuroimaging methods have shown considerable plasticity of MI representations and cell properties following pathological or traumatic changes and in relation to everyday experience, including motor-skill learning and cognitive motor actions. The intrinsic horizontal neuronal connections in MI are a strong candidate substrate for map reorganization: They interconnect large regions of MI, they show activity-dependent plasticity, and they modify in association with skill learning. These findings suggest that MI cortex is not simply a static motor control structure. It also contains a dynamic substrate that participates in motor learning and possibly in cognitive events as well.
Schieber, M. H. "Constraints on Somatotopic Organization in the Primary Motor Cortex." J. Neurophysiol. 86 (2001): 2125-2143.
PubMed abstract: Since the 1870s, the primary motor cortex (M1) has been known to have a somatotopic organization, with different regions of cortex participating in control of face, arm, and leg movements. Through the middle of the 20th century, it seemed possible that the principle of somatotopic organization extended to the detailed representation of different body parts within each of the three major representations. The arm region of M1, for example, was thought to contain a well-ordered, point-to-point representation of the movements or muscles of the thumb, index, middle, ring, and little fingers, the wrist, elbow, and shoulder, as conveyed by the iconic homunculus and simiusculus. In the last quarter of the 20th century, however, experimental evidence has accumulated indicating that within-limb somatotopy in M1 is not spatially discrete nor sequentially ordered. Rather, beneath gradual somatotopic gradients of representation, the representations of different smaller body parts or muscles each are distributed widely within the face, arm, or leg representation, such that the representations of any two smaller parts overlap extensively. Appreciation of this underlying organization will be essential to further understanding of the contribution to control of movement made by M1. Because no single experiment disproves a well-ordered within-limb somatotopic organization in M1, here I review the accumulated evidence, using a framework of six major features that constrain the somatotopic organization of M1: convergence of output, divergence of output, horizontal interconnections, distributed activation, effects of lesions, and ability to reorganize. Review of the classic experiments that led to development of the homunculus and simiusculus shows that these data too were consistent with distributed within-limb somatotopy. I conclude with speculations on what the constrained somatotopy of M1 might tell us about its contribution to control of movement.
Scott, S. H., P. L. Gribble, K. M. Graham, and D. W. Cabel. "Dissociation Between Hand Motion and Population Vectors from Neural Activity in Motor Cortex." Nature 413 (2001): 161-165.
PubMed abstract: The population vector hypothesis was introduced almost twenty years ago to illustrate that a population vector constructed from neural activity in primary motor cortex (MI) of non-human primates could predict the direction of hand movement during reaching. Alternative explanations for this population signal have been suggested but could not be tested experimentally owing to movement complexity in the standard reaching model. We re-examined this issue by recording the activity of neurons in contralateral MI of monkeys while they made reaching movements with their right arms oriented in the horizontal plane-where the mechanics of li