scholarly journals Encoding of limb state by single neurons in the cuneate nucleus of awake monkeys

Author(s):  
Christopher Versteeg ◽  
Joshua M. Rosenow ◽  
Sliman J Bensmaia ◽  
Lee E Miller

The cuneate nucleus (CN) is among the first sites along the neuraxis where proprioceptive signals can be integrated, transformed, and modulated. The objective of the study was to characterize the proprioceptive representations in CN. To this end, we recorded from single CN neurons in three monkeys during active reaching and passive limb perturbation. We found that many neurons exhibited responses that were tuned approximately sinusoidally to limb movement direction, as has been found for other sensorimotor neurons. The distribution of their preferred directions (PDs) was highly non-uniform and resembled that of muscle spindles within individual muscles, suggesting that CN neurons typically receive inputs from only a single muscle. We also found that the responses of proprioceptive CN neurons tended to be modestly amplified during active reaching movements compared to passive limb perturbations, in contrast to cutaneous CN neurons whose responses were not systematically different in the active and passive conditions. Somatosensory signals thus seem to be subject to a "spotlighting" of relevant sensory information rather than uniform suppression as has been suggested previously.

2021 ◽  
Author(s):  
Christopher Versteeg ◽  
Joshua M Rosenow ◽  
Sliman J Bensmaia ◽  
Lee E Miller

The cuneate nucleus (CN) is among the first sites along the neuraxis where proprioceptive signals can be integrated, transformed, and modulated. The objective of the study was to characterize the proprioceptive representations in CN. To this end, we recorded from single CN neurons in three monkeys during active reaching and passive limb perturbation. We found that many neurons exhibited responses that were tuned approximately sinusoidally to limb movement direction, as has been found for other sensorimotor neurons. The distribution of their preferred directions (PDs) was highly non-uniform and resembled that of muscle spindles within individual muscles, suggesting that CN neurons typically receive inputs from only a single muscle. We also found that the responses of proprioceptive CN neurons tended to be modestly amplified during active reaching movements compared to passive limb perturbations, in contrast to cutaneous CN neurons whose responses were not systematically different in the active and passive conditions. Somatosensory signals thus seem to be subject to a 'spotlighting' of relevant sensory information rather than uniform suppression as has been suggested previously.


1999 ◽  
Vol 81 (3) ◽  
pp. 1045-1056 ◽  
Author(s):  
R. L. Sainburg ◽  
C. Ghez ◽  
D. Kalakanis

Intersegmental dynamics are controlled by sequential anticipatory, error correction, and positional control mechanisms. The purpose of this study is to examine the mechanisms underlying control of intersegmental dynamics during reaching movements. Two experiments were conducted to determine the relative contributions of anticipatory and somatosensory feedback mechanisms in controlling intersegmental dynamics and whether adaptation to novel intersegmental dynamics generalizes across a range of movement directions. The mechanisms used to control interaction torques were examined by altering the inertial load of the forearm. Movements were restricted to the shoulder and elbow and supported on a horizontal plane by a frictionless air-jet system. Subjects made rapid out-and-back movements over a target line presented on a computer screen. The screen cursor disappeared at movement onset, and hand paths were displayed after each movement. After subjects adapted to a novel inertial configuration, the position of an attached mass was changed on pseudorandom trials. During these “surprise” trials, movements were initiated with the torque patterns appropriate to the previously learned inertial condition. As a result, characteristic errors in initial movement direction were predicted by an open-looped forward simulation. After these errors occurred, feedback mediated changes in torque emerged that, surprisingly, further decreased the accuracy of movement reversals. Nevertheless at the end of movement, the hand consistently returned to the starting position. It is plausible that the final position was determined completely by feedback-mediated changes in torque. In a second experiment, adaptation to a novel inertial load during movements made in a single direction showed limited transfer across a range of directions. These findings support and extend those of previous reports, which indicated combined anticipatory and postural mechanisms to coordinate rapid reaching movements. The current results indicate a three-stage control system that sequentially links anticipatory, error correction, and postural mechanisms to control intersegmental dynamics. Our results, showing limited generalization across directions, are consistent with previous reports examining adaptation to externally applied forces and extend those findings to indicate that the nervous system uses sensory information to recalibrate internal representations of the musculoskeletal apparatus itself.


1995 ◽  
Vol 73 (6) ◽  
pp. 2563-2567 ◽  
Author(s):  
S. H. Scott ◽  
J. F. Kalaska

1. Neuronal activity was recorded in the motor cortex of a monkey that performed reaching movements with the use of two different arm postures. In the first posture (control), the monkey used its natural arm orientation, approximately in the sagittal plane. In the second posture (abducted), the monkey had to adduct its elbow nearly to shoulder level to grasp the handle. The path of the hand between targets was similar in both arm postures, but the joint kinematics and kinetics were different. 2. In both postures, the activity of single cells was often broadly tuned with movement direction and static arm posture over the targets. In a large proportion of cells, either the level of tonic activity, the directional tuning, or both, varied between the two postures during the movement and target hold periods. 3. For most directions of movement, there was a statistically significant difference in the direction of the population vector for the two arm postures. Furthermore, whereas the population vector tended to point in the direction of movement for the control posture, there was a poorer correspondence between the direction of movement and the population vector for the abducted posture. These observed changes are inconsistent with the notion that the motor cortex encodes purely hand trajectory in space.


1998 ◽  
Vol 80 (3) ◽  
pp. 1132-1150 ◽  
Author(s):  
Driss Boussaoud ◽  
Christophe Jouffrais ◽  
Frank Bremmer

Boussaoud, Driss, Christophe Jouffrais, and Frank Bremmer. Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. J. Neurophysiol. 80: 1132–1150, 1998. Visual inputs to the brain are mapped in a retinocentric reference frame, but the motor system plans movements in a body-centered frame. This basic observation implies that the brain must transform target coordinates from one reference frame to another. Physiological studies revealed that the posterior parietal cortex may contribute a large part of such a transformation, but the question remains as to whether the premotor areas receive visual information, from the parietal cortex, readily coded in body-centered coordinates. To answer this question, we studied dorsal premotor cortex (PMd) neurons in two monkeys while they performed a conditional visuomotor task and maintained fixation at different gaze angles. Visual stimuli were presented on a video monitor, and the monkeys made limb movements on a panel of three touch pads located at the bottom of the monitor. A trial begins when the monkey puts its hand on the central pad. Then, later in the trial, a colored cue instructed a limb movement to the left touch pad if red or to the right one if green. The cues lasted for a variable delay, the instructed delay period, and their offset served as the go signal. The fixation spot was presented at the center of the screen or at one of four peripheral locations. Because the monkey's head was restrained, peripheral fixations caused a deviation of the eyes within the orbit, but for each fixation angle, the instructional cue was presented at nine locations with constant retinocentric coordinates. After the presentation of the instructional cue, 133 PMd cells displayed a phasic discharge (signal-related activity), 157 were tonically active during the instructed delay period (set-related or preparatory activity), and 104 were active after the go signal in relation to movement (movement-related activity). A large proportion of cells showed variations of the discharge rate in relation to limb movement direction, but only modest proportions were sensitive to the cue's location (signal, 43%; set, 34%; movement, 29%). More importantly, the activity of most neurons (signal, 74%; set, 79%; movement, 79%) varied significantly (analysis of variance, P < 0.05) with orbital eye position. A regression analysis showed that the neuronal activity varied linearly with eye position along the horizontal and vertical axes and can be approximated by a two-dimensional regression plane. These data provide evidence that eye position signals modulate the neuronal activity beyond sensory areas, including those involved in visually guided reaching limb movements. Further, they show that neuronal activity related to movement preparation and execution combines at least two directional parameters: arm movement direction and gaze direction in space. It is suggested that a substantial population of PMd cells codes limb movement direction in a head-centered reference frame.


2017 ◽  
Vol 117 (3) ◽  
pp. 1239-1257 ◽  
Author(s):  
Layne H. Salmond ◽  
Andrew D. Davidson ◽  
Steven K. Charles

Smoothness is a hallmark of healthy movement. Past research indicates that smoothness may be a side product of a control strategy that minimizes error. However, this is not the only reason for smooth movements. Our musculoskeletal system itself contributes to movement smoothness: the mechanical impedance (inertia, damping, and stiffness) of our limbs and joints resists sudden change, resulting in a natural smoothing effect. How the biomechanics and neural control interact to result in an observed level of smoothness is not clear. The purpose of this study is to 1) characterize the smoothness of wrist rotations, 2) compare it with the smoothness of planar shoulder-elbow (reaching) movements, and 3) determine the cause of observed differences in smoothness. Ten healthy subjects performed wrist and reaching movements involving different targets, directions, and speeds. We found wrist movements to be significantly less smooth than reaching movements and to vary in smoothness with movement direction. To identify the causes underlying these observations, we tested a number of hypotheses involving differences in bandwidth, signal-dependent noise, speed, impedance anisotropy, and movement duration. Our simulations revealed that proximal-distal differences in smoothness reflect proximal-distal differences in biomechanics: the greater impedance of the shoulder-elbow filters neural noise more than the wrist. In contrast, differences in signal-dependent noise and speed were not sufficiently large to recreate the observed differences in smoothness. We also found that the variation in wrist movement smoothness with direction appear to be caused by, or at least correlated with, differences in movement duration, not impedance anisotropy. NEW & NOTEWORTHY This article presents the first thorough characterization of the smoothness of wrist rotations (flexion-extension and radial-ulnar deviation) and comparison with the smoothness of reaching (shoulder-elbow) movements. We found wrist rotations to be significantly less smooth than reaching movements and determined that this difference reflects proximal-distal differences in biomechanics: the greater impedance (inertia, damping, stiffness) of the shoulder-elbow filters noise in the command signal more than the impedance of the wrist.


1994 ◽  
Vol 72 (5) ◽  
pp. 2280-2301 ◽  
Author(s):  
M. J. Prud'homme ◽  
J. F. Kalaska

1. We studied the activity of 254 cells in the primary somatosensory cortex (SI) responding to inputs from peripheral proprioceptors in a variety of tasks requiring active reaching movements of the contralateral arm. 2. The majority of cells with receptive fields on the proximal arm (shoulder and elbow) were broadly and unimodally tuned for movement direction, often with approximately sinusoidal tuning curves similar to those seen in motor and parietal cortex. 3. The predominant temporal response profiles were directionally tuned phasic bursts during movement and tonic activity that varied with different arm postures. 4. Most cells showed both phasic and tonic response components to differing degrees, and the population formed a continuum from purely phasic to purely tonic cells with no evidence of separate distinct phasic and tonic populations. This indicates that the initial cortical neuronal correlates of the introspectively distinguishable sensations of movement and position are represented in an overlapping or distributed manner in SI. 5. The directional tuning of the phasic and tonic response components of most cells was generally similar, although rarely identical. 6. We tested 62 cells during similar active and passive arm movements. Many cells showed large differences in their responses in the two conditions, presumably due to changes in peripheral receptor discharge during active muscle contractions. 7. We tested 86 cells in a convergent movement task in which monkeys made reaching movements to a single central target from eight peripheral starting positions. A majority of the cells (46 of 86, 53.5%) showed a movement direction-related hysteresis in which their tonic activity after movement to the central target varied with the direction by which the arm moved to the target. The directionality of this hysteresis was coupled with the movement-related directional tuning of the cells. 8. We recorded the discharge of 93 cells as the monkeys performed the task while compensating for loads in different directions. The large majority of cells showed a statistically significant modulation of activity as a function of load direction, which was qualitatively similar to that seen in motor cortex under similar task conditions. Quantitatively, however, the sensitivity of SI proprioceptive cells to loads was less than that seen in motor cortex but greater than in parietal cortex. 9. We interpret these results in terms of their implications for the central representation of the spatiotemporal form (“kinematics”) of arm movements and postures. Most importantly, the results emphasize the important influence of muscle contractile activity on the central proprioceptive representation of active movements.


2017 ◽  
Vol 118 (6) ◽  
pp. 3271-3281 ◽  
Author(s):  
Aneesha K. Suresh ◽  
Jeremy E. Winberry ◽  
Christopher Versteeg ◽  
Raeed Chowdhury ◽  
Tucker Tomlinson ◽  
...  

While the response properties of neurons in the somatosensory nerves and anterior parietal cortex have been extensively studied, little is known about the encoding of tactile and proprioceptive information in the cuneate nucleus (CN) or external cuneate nucleus (ECN), the first recipients of upper limb somatosensory afferent signals. The major challenge in characterizing neural coding in CN/ECN has been to record from these tiny, difficult-to-access brain stem structures. Most previous investigations of CN response properties have been carried out in decerebrate or anesthetized animals, thereby eliminating the well-documented top-down signals from cortex, which likely exert a strong influence on CN responses. Seeking to fill this gap in our understanding of somatosensory processing, we describe an approach to chronically implanting arrays of electrodes in the upper limb representation in the brain stem in primates. First, we describe the topography of CN/ECN in rhesus macaques, including its somatotopic organization and the layout of its submodalities (touch and proprioception). Second, we describe the design of electrode arrays and the implantation strategy to obtain stable recordings. Third, we show sample responses of CN/ECN neurons in brain stem obtained from awake, behaving monkeys. With this method, we are in a position to characterize, for the first time, somatosensory representations in CN and ECN of primates. NEW & NOTEWORTHY In primates, the neural basis of touch and of our sense of limb posture and movements has been studied in the peripheral nerves and in somatosensory cortex, but coding in the cuneate and external cuneate nuclei, the first processing stage for these signals in the central nervous system, remains an enigma. We have developed a method to record from these nuclei, thereby paving the way to studying how sensory information from the limb is encoded there.


2021 ◽  
Vol 11 (6) ◽  
pp. 2615
Author(s):  
Elisa Galofaro ◽  
Erika D’Antonio ◽  
Fabrizio Patané ◽  
Maura Casadio ◽  
Lorenzo Masia

Proprioception—the sense of body segment’s position and movement—plays a crucial role in human motor control, integrating the sensory information necessary for the correct execution of daily life activities. Despite scientific evidence recognizes that several neurological diseases hamper proprioceptive encoding with consequent inability to correctly perform movements, proprioceptive assessment in clinical settings is still limited to standard scales. Literature on physiology of upper limb’s proprioception is mainly focused on experimental approaches involving planar setups, while the present work provides a novel paradigm for assessing proprioception during single—and multi-joint matching tasks in a three-dimensional workspace. To such extent, a six-degrees of freedom exoskeleton, ALEx-RS (Arm Light Exoskeleton Rehab Station), was used to evaluate 18 healthy subjects’ abilities in matching proprioceptive targets during combined single and multi-joint arm’s movements: shoulder abduction/adduction, shoulder flexion/extension, and elbow flexion/extension. Results provided evidence that proprioceptive abilities depend on the number of joints simultaneously involved in the task and on their anatomical location, since muscle spindles work along their preferred direction, modulating the streaming of sensory information accordingly. These findings suggest solutions for clinical sensorimotor evaluation after neurological disease, where assessing proprioceptive deficits can improve the recovery path and complement the rehabilitation outcomes.


2010 ◽  
Vol 104 (5) ◽  
pp. 2654-2666 ◽  
Author(s):  
Gregory A. Apker ◽  
Timothy K. Darling ◽  
Christopher A. Buneo

Reaching movements are subject to noise in both the planning and execution phases of movement production. The interaction of these noise sources during natural movements is not well understood, despite its importance for understanding movement variability in neurologically intact and impaired individuals. Here we examined the interaction of planning and execution related noise during the production of unconstrained reaching movements. Subjects performed sequences of two movements to targets arranged in three vertical planes separated in depth. The starting position for each sequence was also varied in depth with the target plane; thus required movement sequences were largely contained within the vertical plane of the targets. Each final target in a sequence was approached from two different directions, and these movements were made with or without visual feedback of the moving hand. These combined aspects of the design allowed us to probe the interaction of execution and planning related noise with respect to reach endpoint variability. In agreement with previous studies, we found that reach endpoint distributions were highly anisotropic. The principal axes of movement variability were largely aligned with the depth axis, i.e., the axis along which visual planning related noise would be expected to dominate, and were not generally well aligned with the direction of the movement vector. Our results suggest that visual planning–related noise plays a dominant role in determining anisotropic patterns of endpoint variability in three-dimensional space, with execution noise adding to this variability in a movement direction-dependent manner.


2012 ◽  
Vol 115 (1) ◽  
pp. 261-272 ◽  
Author(s):  
Josep Maria Tous-Ral ◽  
Ruben Muiños ◽  
Liudmila Liutsko ◽  
Carlos G. Forero

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