scholarly journals Responses of somatosensory area 2 neurons to actively and passively generated limb movements

2013 ◽  
Vol 109 (6) ◽  
pp. 1505-1513 ◽  
Author(s):  
Brian M. London ◽  
Lee E. Miller

Control of reaching movements requires an accurate estimate of the state of the limb, yet sensory signals are inherently noisy, because of both noise at the receptors themselves and the stochastic nature of the information representation by neural discharge. One way to derive an accurate representation from noisy sensor data is to combine it with the output of a forward model that considers both the previous state estimate and the noisy input. We recorded from primary somatosensory cortex (S1) in macaques ( Macaca mulatta) during both active and passive movements to investigate how the proprioceptive representation of movement in S1 may be modified by the motor command (through efference copy). We found neurons in S1 that respond to one or both movement types covering a broad distribution from active movement only, to both, to passive movement only. Those neurons that responded to both active and passive movements responded with similar directional tuning. Confirming earlier results, some, but not all, neurons responded before the onset of volitional movements, possibly as a result of efference copy. Consequently, many of the features necessary to combine the forward model with proprioceptive feedback appear to be present in S1. These features would not be expected from combinations of afferent receptor responses alone.

1980 ◽  
Vol 44 (6) ◽  
pp. 1122-1138 ◽  
Author(s):  
J. R. Wolpaw

1. Monkeys were trained to maintain hand position against a range of constant forces. Short-latency responses to passive wrist extension or flexion, as well as short-latency responses to stretch of a single wrist muscle, were recorded from units in areas 4, 3, 1, and 2. These responses were compared to unit activity during active holding and during active movement. 2. Units related to active holding and to active movement were most common in areas 4 and 2. Three-quarters of these units displayed a specific correlation between their passive and active behaviors. Thus, a unit excited by passive extension was excited during active holding against extension force and excited during an active flexion movement. This behavior is similar to the expected concurrent behavior of muscle stretch receptors. By demonstrating that a significant number of task-related units give qualitatively similar responses to passive extension and passive flexion, the results appear to explain the disagreement among previous studies (5, 9, 36) in regard to area 4 behavior during active and passive movements. 3. Area 4 units responded similarly to passive wrist extension and electromagnetic stretch of a single flexor muscle occurring in the absence of wrist extension, indicating that muscle stretch was important in determining area 4 unit responses to passive movements. 4. The similarity of area 4 behavior to area 2 behavior in active and passive situations, along with the observation that area 2 responses to passive movements occurred several milliseconds earlier than those of area 4, emphasizes the importance of area 2 in motor performance and is consistent with significant area 2 mediation of area 4 responses. 5. Results support the hypothesis of an oligosynaptic transcortical pathway (22, 32, 34), beginning in large part with muscle stretch receptors. Furthermore, the correlation noted between short-latency responses to passive movement and task-related activity suggests that this transcortical pathway not only mediates responses to passive movement but may be responsible, to a significant degree, for task-related activity during undisturbed performance. Thus, active position maintenance and active movement were probably accomplished, at least in part, by increasing and decreasing the influence of this pathway on specific area 4 neurons and thereby producing the patterns of area 4 activity responsible for task performance.


2019 ◽  
Author(s):  
Konstantina Kilteni ◽  
Patrick Engeler ◽  
H. Henrik Ehrsson

AbstractA self-generated touch feels less intense than an external touch of the exact same intensity. According to a prevalent computational theory of motor control, this attenuation occurs because the brain uses internal forward models to predict the somatosensory consequences of our movements using a copy of the motor command, i.e., the efference copy. These tactile predictions are then used to suppress the perceived intensity of the actual tactile feedback. Despite being highly influential, the core assumption of theory has never been tested; that is, whether the efference copy is necessary for somatosensory attenuation. A possible alternative hypothesis is that a predictable contact of two of one’s own body parts is sufficient. Using a psychophysical task, we quantified the attenuation of touch applied on the participants’ left index finger when the touch was triggered by the active or passive movement of the participants’ right index finger and when it was externally generated in the absence of any movement. We observed somatosensory attenuation only when the touch was triggered by the voluntary movement of the participants’ finger. In contrast, during the passive movement, the intensity of the touch was perceived to be as strong as when the touch was externally triggered. In both active and passive movement conditions, the participants showed the same discrimination capacity. Electromyographic recordings confirmed minimal activity of the right hand during the passive movement. Together, our results suggest that the efference copy is necessary for computing the somatosensory predictions that produce the attenuation of self-generated touch.


2005 ◽  
Vol 93 (3) ◽  
pp. 1304-1316 ◽  
Author(s):  
Joshua P. Bassett ◽  
Michaël B. Zugaro ◽  
Gary M. Muir ◽  
Edward J. Golob ◽  
Robert U. Muller ◽  
...  

Neurons in the anterior dorsal thalamic nucleus (ADN) of the rat selectively discharge in relation to the animal's head direction (HD) in the horizontal plane. Temporal analyses of cell firing properties reveal that their discharge is optimally correlated with the animal's future directional heading by ∼24 ms. Among the hypotheses proposed to explain this property is that ADN HD cells are informed of future head movement via motor efference copy signals. One prediction of this hypothesis is that when the rat's head is moved passively, the anticipatory time interval (ATI) will be attenuated because the motor efference signal reflects only the active contribution to the movement. The present study tested this hypothesis by loosely restraining the animal and passively rotating it through the cell's preferred direction. Contrary to our prediction, we found that ATI values did not decrease during passive movement but in fact increased significantly. HD cells in the postsubiculum did not show the same effect, suggesting independence between the two sites with respect to anticipatory firing. We conclude that it is unlikely that a motor efference copy signal alone is responsible for generating anticipatory firing in ADN HD cells.


2002 ◽  
Vol 88 (4) ◽  
pp. 1968-1979 ◽  
Author(s):  
Stephan R. Williams ◽  
C. Elaine Chapman

This study investigated the relative importance of central and peripheral signals for movement-related gating by comparing the time course and magnitude of movement-related decreases in tactile detection during a reference motor task, active isotonic digit 2 (D2) abduction, with that seen during three test tasks: a comparison with active isometric D2 abduction (movement vs. no movement) evaluated the contribution of peripheral reafference generated by the movement to gating; a comparison with passive D2 abduction (motor command vs. no motor command; movement generated by an external agent) allowed us to evaluate the contribution of the central motor command to tactile gating; and finally, the inclusion of an active “no apparatus,” or freehand, D2 abduction task allowed us to evaluate the potential contribution of incidental peripheral reafference generated by the position detecting apparatus to the results (apparatus vs. no apparatus). Weak electrical stimuli (2-ms pulse; intensity, 90% detected at rest) were applied to D2 at different delays before and after movement onset or electromyographic (EMG) activity onset. Significant time-dependent movement-related decreases in detection were obtained with all tasks. When the results obtained during the active isotonic movement task were compared with those obtained in the three test tasks, no significant differences in the functions describing detection performance over time were seen. The results obtained with the isometric D2 abduction task show that actual movement of a body part is not necessary to diminish detection of tactile stimuli in a manner similar to the decrease produced by isotonic, active movement. In the passive test task, the peak decrease in detection clearly preceded the onset of passive movement (by 38 ms) despite the lack of a motor command and, presumably, no movement-related peripheral reafference. A slightly but not significantly earlier decrease was obtained with active movement (49 ms before movement onset). Expectation of movement likely did not contribute to the results because stimulus detection during sham passive movement trials (subjects expected but did not receive a passive movement) was not different from performance at rest (no movement). The results obtained with passive movement are best explained by invoking backward masking of the test stimuli by movement-related reafference and demonstrate that movement-related reafference is sufficient to produce decreases in detection with a time course and amplitude not significantly different from that produced by active movement.


1980 ◽  
Vol 44 (6) ◽  
pp. 1139-1147 ◽  
Author(s):  
J. R. Wolpaw

1. Monkeys learned to maintain hand position against a range of background forces. Short-latency responses to passive wrist extension or flexion were recorded from units in areas 4, 3, 1, and 2. Response amplitude was studied as a function of background force direction (extension or flexion). 2. For 40% of the precentral and postcentral responses, response amplitude depended on constant force direction. For these dependent responses, amplitude with background force in one direction averaged 2.8 times amplitude with background force in the opposite direction. 3. Units for which background activity varied with constant force direction were designated task related. Dependent responses from area 4 task-related units were usually larger when background activity was greater and when background force direction matched the direction of the passive movement. 4. Dependent responses from area 4 task-related units occurred significantly later than nondependent responses from the same units. 5. Since most area 4 task-related activity was explicable as a result of peripheral input via the same oligosynaptic path mediating area 4 responses to passive movements (32), the present findings imply that area 4-task-related activity may result in large part from centrally mediated change in the access of short-latency peripheral input to area 4 units. 6. The dependence of responses from non-task-related area 4 units and from non-task-related and task-related postcentral units showed no dominant correlation with background activity or with background force direction. Their dependence appeared to require no explanation other than a change in peripheral input with change in background force direction.


2020 ◽  
Author(s):  
Sheo Shankar Pandey ◽  
Fernanda N.C. Vasconcelos ◽  
Nian Wang

Candidatus Liberibacter asiaticus (CLas), the causal agent of citrus huanglongbing, colonizes inside the phloem and is naturally transmitted by the Asian citrus psyllid (ACP). Here, we investigated the spatiotemporal CLas colonization in different tissues post ACP transmission. At 75 day-post-ACP-removal (DPR), CLas was detected in roots of all trees, but in the mature leaf of only one tree, of the nine plants that were successfully infected via ACP transmission, consistent with the model that CLas moves passively from the source to sink. CLas was detected in 11.1%, and 43.1% mature leaves, which were unfed by ACPs during transmission, at 75, and 365 DPR, respectively, unveiling active movement to the source tissue. The difference in colonization timing of sink and source tissues indicates CLas is capable of both passive and active movement with passive movement being dominant. At 225 DPR, leaves fed by ACPs during the young stage showed the highest ratio of HLB symptomatic leaves and highest CLas titer, followed by that of leaves emerged post ACP removal, and mature leaves not fed by ACPs. Importantly, our data showed that ACPs were unable to transmit CLas via feeding on mature leaves. It is estimated that it takes at most three years for CLas to infect the whole tree. Overall, the spatiotemporal detection of CLas in different tissues after ACP transmission helps visualize the infection process of CLas in planta and subsequent HLB symptom development, and provides the knowledge supporting that young leaves should be the focus of HLB management.


2009 ◽  
Vol 101 (1) ◽  
pp. 141-149 ◽  
Author(s):  
Mohsen Jamali ◽  
Soroush G. Sadeghi ◽  
Kathleen E. Cullen

The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self- or externally generated.


1975 ◽  
Vol 40 (3) ◽  
pp. 755-761 ◽  
Author(s):  
Brian Craske ◽  
Martin Crawshaw

The position sense of a stationary arm was investigated subsequent to an horizontally adductive movement with axis the shoulder joint. The right arm was the treated arm: it reached a test position actively, using minimal voluntary effort, or passively from each of 10 starting positions. The blindfolded S localized the index finger of the treated arm by attempting to touch it with the index finger of his left hand. The results indicate that subsequent to active movement the final position of a limb is more accurately known than a position resulting from passive movement. A second finding is that concomitant with both forms of limb placement there is a unidirectional drift of perceived limb position over trials.


2016 ◽  
Vol 116 (4) ◽  
pp. 1831-1839 ◽  
Author(s):  
Marc Benazet ◽  
François Thénault ◽  
Kevin Whittingstall ◽  
Pierre-Michel Bernier

It is well established that the cortical processing of somatosensory and auditory signals is attenuated when they result from self-generated actions compared with external events. This phenomenon is thought to result from an efference copy of motor commands used to predict the sensory consequences of an action through a forward model. The present work examined whether attenuation also takes place for visual reafferent signals from the moving limb during voluntary reaching movements. To address this issue, EEG activity was recorded in a condition in which visual feedback of the hand was provided in real time and compared with a condition in which it was presented with a 150-ms delay, thus creating a mismatch between the predicted and actual visual consequences of the movement. Results revealed that the amplitude of the N1 component of the visual event-related potential evoked by hand visual feedback over the parietal cortex was significantly smaller when presented in real time compared with when it was delayed. These data suggest that the cortical processing of visual reafferent signals is attenuated when they are correctly predicted, likely as a result of a forward model.


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