Andrew Fuglevand - Academia.edu (original) (raw)

Papers by Andrew Fuglevand

ENeuro, Sep 1, 2016

The majority of neurophysiological studies that have explored the role of the primate amygdala in... more The majority of neurophysiological studies that have explored the role of the primate amygdala in the evaluation of social signals have relied on visual stimuli such as images of facial expressions. Vision, however, is not the only sensory modality that carries social signals. Both humans and nonhuman primates exchange emotionally meaningful social signals through touch. Indeed, social grooming in nonhuman primates and caressing touch in humans is critical for building lasting and reassuring social bonds. To determine the role of the amygdala in processing touch, we recorded the responses of single neurons in the macaque amygdala while we applied tactile stimuli to the face. We found that one-third of the recorded neurons responded to tactile stimulation. Although we recorded exclusively from the right amygdala, the receptive fields of 98% of the neurons were bilateral. A fraction of these tactile neurons were monitored during the production of facial expressions and during facial movements elicited occasionally by touch stimuli. Firing rates arising during the production of facial expressions were similar to those elicited by tactile stimulation. In a subset of cells, combining tactile stimulation with facial movement further augmented the firing rates. This suggests that tactile neurons in the amygdala receive input from skin mechanoceptors that are activated by touch and by compressions and stretches of the facial skin during the contraction of the underlying muscles. Tactile neurons in the amygdala may play a role in extracting the valence of touch stimuli and/or monitoring the facial expressions of self during social interactions.

Physiology & Behavior, Sep 1, 2008

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psyc... more The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans were stimulated successfully in the rhesus macaque and caused similar appearance changes to human facial movements. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from that of monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

Current opinion in behavioral sciences, Feb 1, 2022

The amygdala plays a central role in socio-emotional behavior, yet its role in processing affecti... more The amygdala plays a central role in socio-emotional behavior, yet its role in processing affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala. The connectivity of the amygdala is well-suited to process the sensory features and the socio-cognitive dimensions of touch. The convergent processing of bottom-up and top-down touch-related inputs in the amygdala triggers autonomic responses. The positive hedonic value of touch in humans and grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming reduces vigilance that has been shown to depend critically on the amygdala. Touch-induced vagal tone and lowered vigilance alter neural activity in the amygdala. Under these circumstances neurons no longer respond to each touch stimulus, rather they appear to signal a sustained functional state in which the amygdala appears decoupled from monitoring the external environment.

Journal of Neural Engineering, Sep 17, 2018

Experimental Brain Research, Jun 26, 2004

Evidence from five-digit grasping studies indicates that grip forces exerted by pairs of digits t... more Evidence from five-digit grasping studies indicates that grip forces exerted by pairs of digits tend to be synchronized. It has been suggested that motor unit synchronization might be a mechanism responsible for constraining the temporal relationships between grip forces. To evaluate this possibility and quantify the effect of motor unit synchrony on force relationships, we used a motor unit model to simulate force produced by two muscles using three physiological levels of motor unit synchrony across the two muscles. In one condition, motor units in the two muscles discharged independently of one another. In the other two conditions, the timing of randomly selected motor unit discharges in one muscle was adjusted to impose low or high levels of synchrony with motor units in the other muscle. Fast Fourier transform analysis was performed to compute the phase differences between forces from 0.5 to 17 Hz. We used circular statistics to assess whether the phase differences at each frequency were randomly or non-randomly distributed (Rayleigh test). The mean phase difference was then computed on the non-random distributions. We found that the number of significant phase-difference distributions increased markedly with increasing synchronization strength from 18% for no synchrony to 65% and 82% for modest and strong synchrony conditions, respectively. Importantly, most of the mean angles clustered at very small phase difference values (∼0 to 10°), indicating a strong tendency for forces to be exerted in a synchronous fashion. These results suggest that motor unit synchronization could play a significant functional role in the coordination of grip forces.

Journal of Neural Engineering, Jan 19, 2011

Wiley Interdisciplinary Reviews: Cognitive Science, Aug 11, 2017

A major challenge of primate neurophysiology, particularly in the domain of social neuroscience, ... more A major challenge of primate neurophysiology, particularly in the domain of social neuroscience, is to adopt more natural behaviors without compromising the ability to relate patterns of neural activity to specific actions or sensory inputs. Traditional approaches have identified neural activity patterns in the amygdala in response to simplified versions of social stimuli such as static images of faces. As a departure from this reduced approach, single images of faces were replaced with arrays of images or videos of conspecifics. These stimuli elicited more natural behaviors and new types of neural responses: (1) attention-gated responses to faces, (2) selective responses to eye contact, and (3) selective responses to touch and somatosensory feedback during the production of facial expressions. An additional advance toward more natural social behaviors in the laboratory was the implementation of dyadic social interactions. Under these conditions, neurons encoded similarly rewards that monkeys delivered to self and to their social partner. These findings reinforce the value of bringing natural, ethologically valid, behavioral tasks under neurophysiological scrutiny.

Journal of Neurophysiology

To understand how the central nervous system (CNS) enacts movements, it seems important to monito... more To understand how the central nervous system (CNS) enacts movements, it seems important to monitor the activities of the many muscles involved. Likewise, to restore complex movements to paralyzed limbs with electrical stimulation requires access to most limb muscles. Intramuscular electrodes are needed to obtain isolated recordings or stimulation of individual muscles. As such, we developed and tested the stability of large arrays of implanted intramuscular electrodes. We implanted 58 electrodes in 29 upper limb muscles in each of three macaques. Electrode connectors were protected within a skull-mounted chamber. During surgery, wires were tunneled subcutaneously to target muscles, where gold anchors were crimped onto the leads. The anchors were then deployed with an insertion device. In two monkeys, the chamber was fixed to the skull with a titanium baseplate rather than acrylic cement. In multiple sessions up to 15 wk after surgery, electromyographic (EMG) signals were recorded wh...

SSRN Electronic Journal

SUMMARYThe skin transmits affective signals that integrate into our social vocabulary. As the soc... more SUMMARYThe skin transmits affective signals that integrate into our social vocabulary. As the socio-affective aspects of touch are likely processed in the amygdala, we compared neural responses to social grooming and gentle airflow recorded from the amygdala and the primary somatosensory cortex of non-human primates. Neurons in the somatosensory cortex responded to both types of tactile stimuli. In the amygdala, however, neurons did not respond to individual grooming sweeps even though grooming elicited autonomic states indicative of positive affect. Instead, many showed changes in baseline firing rates that persisted throughout the grooming bout. Such baseline fluctuations were attributed to social context because the presence of the groomer alone could account for the observed changes in baseline activity. It appears, therefore, that during grooming, the amygdala stops responding to external inputs on a short time scale but remains responsive to social context (or the associated affective states) on longer time scales.

Functional electrical stimulation (FES) involves artificial activation of skeletal muscles to rei... more Functional electrical stimulation (FES) involves artificial activation of skeletal muscles to reinstate motor function in paralyzed individuals. While FES applied to the upper limb has improved the ability of tetraplegics to perform activities of daily living, there are key shortcomings impeding its widespread use. One major limitation is that the range of motor behaviors that can be generated is restricted to a small set of simple, preprogrammed movements. This limitation stems from the substantial difficulty in determining the patterns of stimulation across many muscles required to produce more complex movements. Here we show that machine learning can be used to flexibly identify patterns of muscle stimulation needed to evoke a wide array of multi-joint arm movements. Those patterns were delivered concurrently to 29 upper limb muscles in temporarily paralyzed monkeys. In some cases, the evoked responses matched the desired movements with good fidelity. Because the range of movemen...

The amygdala plays a central role in socio-emotional behavior, yet its role in processing affecti... more The amygdala plays a central role in socio-emotional behavior, yet its role in processing affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala. The connectivity of the amygdala is well-suited to process the sensory features and the socio-cognitive dimensions of touch. The convergent processing of bottom-up and top-down touch-related inputs in the amygdala triggers autonomic responses. The positive hedonic value of touch in humans and grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming reduces vigilance that has been shown to depend critically on the amygdala. Touch-induced vagal tone and lowered vigilance alter neural activity in the amygdala. Under these circumstances neurons no longer respond to each touch stimulus, rather they appear to signal a sustained f...

Journal of Neural Engineering, 2018

Objective.-Restoration of motor function in paralyzed limbs using functional electrical stimulati... more Objective.-Restoration of motor function in paralyzed limbs using functional electrical stimulation (FES) is undermined by rapid fatigue associated with artificial stimulation. Typically, single electrodes are used to activate muscles with FES. However, due to the highly distributed branching of muscle nerves, a single electrode may not be able to activate the entire array of motor axons supplying a muscle. Therefore, stimulating muscle with multiple electrodes might enable access to a larger volume of muscle and thereby reduce fatigue. Approach.-Accordingly, we compared the endurance times that ankle dorsiflexion could be sustained at 20% maximum voluntary force using feedback controlled stimulation (25 Hz) of human tibialis anterior (TA) using one or four percutaneous intramuscular electrodes. In addition, we measured endurance times in response to direct stimulation of the nerve supplying TA and during voluntary contraction. In all sessions involving electrical stimulation, an anesthetic nerve block proximal to the site of stimulation was used to isolate the effects of stimulation and alleviate discomfort. Main results.-Endurance time associated with stimuli delivered by a single intramuscular electrode (84 ± 19 s) was significantly smaller than that elicited by four intramuscular electrodes (232 ± 123 s). Moreover, endurance time in response to nerve stimulation (787 ± 201 s) was not significantly different that that produced during voluntary contraction (896 ± 272 s). Significance.-Therefore, excessive fatigue associated with FES is probably due to the inability of conventional FES systems to enlist the full complement of motor axons innervating muscle and can be mitigated using multiple electrodes or nerve-based electrodes.

The Journal of Neuroscience, 2002

Various computational approaches have been applied to predict aspects of animal behavior from the... more Various computational approaches have been applied to predict aspects of animal behavior from the recorded activity of populations of neurons. Here we invert this process to predict the requisite neuromuscular activity associated with specified motor behaviors. A probabilistic method based on Bayes' theorem was used to predict the patterns of muscular activity needed to produce various types of desired finger movements. The profiles of predicted activity were then used to drive frequency-modulated muscle stimulators to evoke multijoint finger movements. Comparison of movements generated by electrical stimulation with desired movements yielded root mean squared errors between ϳ18 and 26%. This reasonable correspondence between desired and evoked movements suggests that this approach might serve as a useful strategy to control neuroprosthetic systems that aim to restore movement to paralyzed individuals.

Journal of Neural Engineering, 2018

Objective. The maximum muscle forces that can be evoked using functional electrical stimulation (... more Objective. The maximum muscle forces that can be evoked using functional electrical stimulation (FES) are relatively modest. The reason for this weakness is not fully understood but could be partly related to the widespread distribution of motor nerve branches within muscle. As such, a single stimulating electrode (as is conventionally used) may be incapable of activating the entire array of motor axons supplying a muscle. Therefore, the objective of this study was to determine whether stimulating a muscle with more than one source of current could boost force above that achievable with a single source. Approach. We compared the maximum isometric forces that could be evoked in the anterior deltoid of anesthetized monkeys using one or two intramuscular electrodes. We also evaluated whether temporally interleaved stimulation between two electrodes might reduce fatigue during prolonged activity compared to synchronized stimulation through two electrodes. Main results. We found that dua...

Journal of Neurophysiology, 2015

The maximum firing rates of motoneurons (MNs), activated in response to synaptic drive, appear to... more The maximum firing rates of motoneurons (MNs), activated in response to synaptic drive, appear to be much lower than that elicited by current injection. It could be that the decrease in input resistance associated with increased synaptic activity (but not current injection) might blunt overall changes in membrane depolarization and thereby limit spike-frequency output. To test this idea, we recorded, in the same cells, maximal firing responses to current injection and to synaptic activation. We prepared 300 μm medullary slices in neonatal rats that contained hypoglossal MNs and used whole-cell patch-clamp electrophysiology to record their maximum firing rates in response to triangular-ramp current injections and to glutamate receptor-mediated excitation. Brief pressure pulses of high-concentration glutamate led to significant depolarization, high firing rates, and temporary cessation of spiking due to spike inactivation. In the same cells, we applied current clamp protocols that app...

Journal of neuroengineering and rehabilitation, Jan 15, 2015

Accurate prediction of electromyographic (EMG) signals associated with a variety of motor behavio... more Accurate prediction of electromyographic (EMG) signals associated with a variety of motor behaviors could, in theory, serve as activity templates needed to evoke movements in paralyzed individuals using functional electrical stimulation. Such predictions should encompass complex multi-joint movements and include interactions with objects in the environment. Here we tested the ability of different artificial neural networks (ANNs) to predict EMG activities of 12 arm muscles while human subjects made free movements of the arm or grasped and moved objects of different weights and dimensions. Inputs to the trained ANNs included hand position, hand orientation, and thumb grip force. The ability of ANNs to predict EMG was equally as good for tasks involving interactions with external loads as for unloaded movements. The ANN that yielded the best predictions was a feed-forward network consisting of a single hidden layer of 30 neural elements. For this network, the average coefficient of de...

The Journal of Physiology, 2003

Motor unit discharge rates decline by about 50 % over 60 s of a sustained maximum voluntary contr... more Motor unit discharge rates decline by about 50 % over 60 s of a sustained maximum voluntary contraction (MVC). It has been suggested that this decline in discharge rate serves to maintain force by protecting against conduction failure and by optimizing the input to motor units as their contractile properties change. This hypothesis, known as muscle wisdom, is based in part on studies in which muscle force was shown to decline more rapidly when stimulation was maintained at a high rate than when stimulus rate was reduced over time. The stimulus rates used in those studies, however, were higher than those normally encountered during MVCs. The purpose of this study was to compare force loss under constant and declining stimulus rate conditions using rates similar to those that occur during voluntary effort. Isometric force and surface EMG signals were recorded from human adductor pollicis muscles in response to supramaximal stimuli delivered to the ulnar nerve at the elbow. Three fatig...

The Journal of Physiology, 2011

Motor units serve both as the mechanical apparatus and the final stage of neural processing thr... more Motor units serve both as the mechanical apparatus and the final stage of neural processing through which motor behaviours are enacted. Therefore, knowledge about the contractile properties and organization of the neural inputs to motor units supplying finger muscles is essential for understanding the control strategies underlying the diverse motor functions of the human hand. In this brief review, basic contractile properties of motor units residing in human hand muscles are described. Hand motor units are not readily categorized into the classical physiological types as established in the cat gastrocnemius muscle. In addition, the distribution of descending synaptic inputs to motor nuclei supplying different hand muscles is outlined. Motor neurons innervating intrinsic muscles appear to have relatively independent lines of input from supraspinal centres whereas substantial divergence of descending input is seen across motor nuclei supplying extrinsic hand muscles. The functional...

The Journal of Neuroscience, 2005

Short-term synchrony was measured for pairs of motor units located within and across muscles acti... more Short-term synchrony was measured for pairs of motor units located within and across muscles activated during a task that mimicked precision grip in the dominant and nondominant hands of human subjects. Surprisingly, synchrony for pairs of motor units residing in separate muscles (flexor pollicis longus, a thumb muscle, and flexor digitorum profundus, an index-finger muscle) was just as large as that for pairs of units both within the thumb muscle. Furthermore, the high level of synchrony seen across muscles in the dominant hand was absent in the nondominant hand. These results suggest that descending pathways diverge to provide extensive common input across motor nuclei involved in the precision grip and that such divergence might contribute to the preferred use of one hand over the other.

Physiology & Behavior, 2008

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psyc... more The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans were stimulated successfully in the rhesus macaque and caused similar appearance changes to human facial movements. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from that of monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

ENeuro, Sep 1, 2016

The majority of neurophysiological studies that have explored the role of the primate amygdala in... more The majority of neurophysiological studies that have explored the role of the primate amygdala in the evaluation of social signals have relied on visual stimuli such as images of facial expressions. Vision, however, is not the only sensory modality that carries social signals. Both humans and nonhuman primates exchange emotionally meaningful social signals through touch. Indeed, social grooming in nonhuman primates and caressing touch in humans is critical for building lasting and reassuring social bonds. To determine the role of the amygdala in processing touch, we recorded the responses of single neurons in the macaque amygdala while we applied tactile stimuli to the face. We found that one-third of the recorded neurons responded to tactile stimulation. Although we recorded exclusively from the right amygdala, the receptive fields of 98% of the neurons were bilateral. A fraction of these tactile neurons were monitored during the production of facial expressions and during facial movements elicited occasionally by touch stimuli. Firing rates arising during the production of facial expressions were similar to those elicited by tactile stimulation. In a subset of cells, combining tactile stimulation with facial movement further augmented the firing rates. This suggests that tactile neurons in the amygdala receive input from skin mechanoceptors that are activated by touch and by compressions and stretches of the facial skin during the contraction of the underlying muscles. Tactile neurons in the amygdala may play a role in extracting the valence of touch stimuli and/or monitoring the facial expressions of self during social interactions.

Physiology & Behavior, Sep 1, 2008

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psyc... more The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans were stimulated successfully in the rhesus macaque and caused similar appearance changes to human facial movements. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from that of monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

Current opinion in behavioral sciences, Feb 1, 2022

The amygdala plays a central role in socio-emotional behavior, yet its role in processing affecti... more The amygdala plays a central role in socio-emotional behavior, yet its role in processing affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala. The connectivity of the amygdala is well-suited to process the sensory features and the socio-cognitive dimensions of touch. The convergent processing of bottom-up and top-down touch-related inputs in the amygdala triggers autonomic responses. The positive hedonic value of touch in humans and grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming reduces vigilance that has been shown to depend critically on the amygdala. Touch-induced vagal tone and lowered vigilance alter neural activity in the amygdala. Under these circumstances neurons no longer respond to each touch stimulus, rather they appear to signal a sustained functional state in which the amygdala appears decoupled from monitoring the external environment.

Journal of Neural Engineering, Sep 17, 2018

Experimental Brain Research, Jun 26, 2004

Evidence from five-digit grasping studies indicates that grip forces exerted by pairs of digits t... more Evidence from five-digit grasping studies indicates that grip forces exerted by pairs of digits tend to be synchronized. It has been suggested that motor unit synchronization might be a mechanism responsible for constraining the temporal relationships between grip forces. To evaluate this possibility and quantify the effect of motor unit synchrony on force relationships, we used a motor unit model to simulate force produced by two muscles using three physiological levels of motor unit synchrony across the two muscles. In one condition, motor units in the two muscles discharged independently of one another. In the other two conditions, the timing of randomly selected motor unit discharges in one muscle was adjusted to impose low or high levels of synchrony with motor units in the other muscle. Fast Fourier transform analysis was performed to compute the phase differences between forces from 0.5 to 17 Hz. We used circular statistics to assess whether the phase differences at each frequency were randomly or non-randomly distributed (Rayleigh test). The mean phase difference was then computed on the non-random distributions. We found that the number of significant phase-difference distributions increased markedly with increasing synchronization strength from 18% for no synchrony to 65% and 82% for modest and strong synchrony conditions, respectively. Importantly, most of the mean angles clustered at very small phase difference values (∼0 to 10°), indicating a strong tendency for forces to be exerted in a synchronous fashion. These results suggest that motor unit synchronization could play a significant functional role in the coordination of grip forces.

Journal of Neural Engineering, Jan 19, 2011

Wiley Interdisciplinary Reviews: Cognitive Science, Aug 11, 2017

A major challenge of primate neurophysiology, particularly in the domain of social neuroscience, ... more A major challenge of primate neurophysiology, particularly in the domain of social neuroscience, is to adopt more natural behaviors without compromising the ability to relate patterns of neural activity to specific actions or sensory inputs. Traditional approaches have identified neural activity patterns in the amygdala in response to simplified versions of social stimuli such as static images of faces. As a departure from this reduced approach, single images of faces were replaced with arrays of images or videos of conspecifics. These stimuli elicited more natural behaviors and new types of neural responses: (1) attention-gated responses to faces, (2) selective responses to eye contact, and (3) selective responses to touch and somatosensory feedback during the production of facial expressions. An additional advance toward more natural social behaviors in the laboratory was the implementation of dyadic social interactions. Under these conditions, neurons encoded similarly rewards that monkeys delivered to self and to their social partner. These findings reinforce the value of bringing natural, ethologically valid, behavioral tasks under neurophysiological scrutiny.

Journal of Neurophysiology

To understand how the central nervous system (CNS) enacts movements, it seems important to monito... more To understand how the central nervous system (CNS) enacts movements, it seems important to monitor the activities of the many muscles involved. Likewise, to restore complex movements to paralyzed limbs with electrical stimulation requires access to most limb muscles. Intramuscular electrodes are needed to obtain isolated recordings or stimulation of individual muscles. As such, we developed and tested the stability of large arrays of implanted intramuscular electrodes. We implanted 58 electrodes in 29 upper limb muscles in each of three macaques. Electrode connectors were protected within a skull-mounted chamber. During surgery, wires were tunneled subcutaneously to target muscles, where gold anchors were crimped onto the leads. The anchors were then deployed with an insertion device. In two monkeys, the chamber was fixed to the skull with a titanium baseplate rather than acrylic cement. In multiple sessions up to 15 wk after surgery, electromyographic (EMG) signals were recorded wh...

SSRN Electronic Journal

SUMMARYThe skin transmits affective signals that integrate into our social vocabulary. As the soc... more SUMMARYThe skin transmits affective signals that integrate into our social vocabulary. As the socio-affective aspects of touch are likely processed in the amygdala, we compared neural responses to social grooming and gentle airflow recorded from the amygdala and the primary somatosensory cortex of non-human primates. Neurons in the somatosensory cortex responded to both types of tactile stimuli. In the amygdala, however, neurons did not respond to individual grooming sweeps even though grooming elicited autonomic states indicative of positive affect. Instead, many showed changes in baseline firing rates that persisted throughout the grooming bout. Such baseline fluctuations were attributed to social context because the presence of the groomer alone could account for the observed changes in baseline activity. It appears, therefore, that during grooming, the amygdala stops responding to external inputs on a short time scale but remains responsive to social context (or the associated affective states) on longer time scales.

Functional electrical stimulation (FES) involves artificial activation of skeletal muscles to rei... more Functional electrical stimulation (FES) involves artificial activation of skeletal muscles to reinstate motor function in paralyzed individuals. While FES applied to the upper limb has improved the ability of tetraplegics to perform activities of daily living, there are key shortcomings impeding its widespread use. One major limitation is that the range of motor behaviors that can be generated is restricted to a small set of simple, preprogrammed movements. This limitation stems from the substantial difficulty in determining the patterns of stimulation across many muscles required to produce more complex movements. Here we show that machine learning can be used to flexibly identify patterns of muscle stimulation needed to evoke a wide array of multi-joint arm movements. Those patterns were delivered concurrently to 29 upper limb muscles in temporarily paralyzed monkeys. In some cases, the evoked responses matched the desired movements with good fidelity. Because the range of movemen...

The amygdala plays a central role in socio-emotional behavior, yet its role in processing affecti... more The amygdala plays a central role in socio-emotional behavior, yet its role in processing affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala. The connectivity of the amygdala is well-suited to process the sensory features and the socio-cognitive dimensions of touch. The convergent processing of bottom-up and top-down touch-related inputs in the amygdala triggers autonomic responses. The positive hedonic value of touch in humans and grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming reduces vigilance that has been shown to depend critically on the amygdala. Touch-induced vagal tone and lowered vigilance alter neural activity in the amygdala. Under these circumstances neurons no longer respond to each touch stimulus, rather they appear to signal a sustained f...

Journal of Neural Engineering, 2018

Objective.-Restoration of motor function in paralyzed limbs using functional electrical stimulati... more Objective.-Restoration of motor function in paralyzed limbs using functional electrical stimulation (FES) is undermined by rapid fatigue associated with artificial stimulation. Typically, single electrodes are used to activate muscles with FES. However, due to the highly distributed branching of muscle nerves, a single electrode may not be able to activate the entire array of motor axons supplying a muscle. Therefore, stimulating muscle with multiple electrodes might enable access to a larger volume of muscle and thereby reduce fatigue. Approach.-Accordingly, we compared the endurance times that ankle dorsiflexion could be sustained at 20% maximum voluntary force using feedback controlled stimulation (25 Hz) of human tibialis anterior (TA) using one or four percutaneous intramuscular electrodes. In addition, we measured endurance times in response to direct stimulation of the nerve supplying TA and during voluntary contraction. In all sessions involving electrical stimulation, an anesthetic nerve block proximal to the site of stimulation was used to isolate the effects of stimulation and alleviate discomfort. Main results.-Endurance time associated with stimuli delivered by a single intramuscular electrode (84 ± 19 s) was significantly smaller than that elicited by four intramuscular electrodes (232 ± 123 s). Moreover, endurance time in response to nerve stimulation (787 ± 201 s) was not significantly different that that produced during voluntary contraction (896 ± 272 s). Significance.-Therefore, excessive fatigue associated with FES is probably due to the inability of conventional FES systems to enlist the full complement of motor axons innervating muscle and can be mitigated using multiple electrodes or nerve-based electrodes.

The Journal of Neuroscience, 2002

Various computational approaches have been applied to predict aspects of animal behavior from the... more Various computational approaches have been applied to predict aspects of animal behavior from the recorded activity of populations of neurons. Here we invert this process to predict the requisite neuromuscular activity associated with specified motor behaviors. A probabilistic method based on Bayes' theorem was used to predict the patterns of muscular activity needed to produce various types of desired finger movements. The profiles of predicted activity were then used to drive frequency-modulated muscle stimulators to evoke multijoint finger movements. Comparison of movements generated by electrical stimulation with desired movements yielded root mean squared errors between ϳ18 and 26%. This reasonable correspondence between desired and evoked movements suggests that this approach might serve as a useful strategy to control neuroprosthetic systems that aim to restore movement to paralyzed individuals.

Journal of Neural Engineering, 2018

Objective. The maximum muscle forces that can be evoked using functional electrical stimulation (... more Objective. The maximum muscle forces that can be evoked using functional electrical stimulation (FES) are relatively modest. The reason for this weakness is not fully understood but could be partly related to the widespread distribution of motor nerve branches within muscle. As such, a single stimulating electrode (as is conventionally used) may be incapable of activating the entire array of motor axons supplying a muscle. Therefore, the objective of this study was to determine whether stimulating a muscle with more than one source of current could boost force above that achievable with a single source. Approach. We compared the maximum isometric forces that could be evoked in the anterior deltoid of anesthetized monkeys using one or two intramuscular electrodes. We also evaluated whether temporally interleaved stimulation between two electrodes might reduce fatigue during prolonged activity compared to synchronized stimulation through two electrodes. Main results. We found that dua...

Journal of Neurophysiology, 2015

The maximum firing rates of motoneurons (MNs), activated in response to synaptic drive, appear to... more The maximum firing rates of motoneurons (MNs), activated in response to synaptic drive, appear to be much lower than that elicited by current injection. It could be that the decrease in input resistance associated with increased synaptic activity (but not current injection) might blunt overall changes in membrane depolarization and thereby limit spike-frequency output. To test this idea, we recorded, in the same cells, maximal firing responses to current injection and to synaptic activation. We prepared 300 μm medullary slices in neonatal rats that contained hypoglossal MNs and used whole-cell patch-clamp electrophysiology to record their maximum firing rates in response to triangular-ramp current injections and to glutamate receptor-mediated excitation. Brief pressure pulses of high-concentration glutamate led to significant depolarization, high firing rates, and temporary cessation of spiking due to spike inactivation. In the same cells, we applied current clamp protocols that app...

Journal of neuroengineering and rehabilitation, Jan 15, 2015

Accurate prediction of electromyographic (EMG) signals associated with a variety of motor behavio... more Accurate prediction of electromyographic (EMG) signals associated with a variety of motor behaviors could, in theory, serve as activity templates needed to evoke movements in paralyzed individuals using functional electrical stimulation. Such predictions should encompass complex multi-joint movements and include interactions with objects in the environment. Here we tested the ability of different artificial neural networks (ANNs) to predict EMG activities of 12 arm muscles while human subjects made free movements of the arm or grasped and moved objects of different weights and dimensions. Inputs to the trained ANNs included hand position, hand orientation, and thumb grip force. The ability of ANNs to predict EMG was equally as good for tasks involving interactions with external loads as for unloaded movements. The ANN that yielded the best predictions was a feed-forward network consisting of a single hidden layer of 30 neural elements. For this network, the average coefficient of de...

The Journal of Physiology, 2003

Motor unit discharge rates decline by about 50 % over 60 s of a sustained maximum voluntary contr... more Motor unit discharge rates decline by about 50 % over 60 s of a sustained maximum voluntary contraction (MVC). It has been suggested that this decline in discharge rate serves to maintain force by protecting against conduction failure and by optimizing the input to motor units as their contractile properties change. This hypothesis, known as muscle wisdom, is based in part on studies in which muscle force was shown to decline more rapidly when stimulation was maintained at a high rate than when stimulus rate was reduced over time. The stimulus rates used in those studies, however, were higher than those normally encountered during MVCs. The purpose of this study was to compare force loss under constant and declining stimulus rate conditions using rates similar to those that occur during voluntary effort. Isometric force and surface EMG signals were recorded from human adductor pollicis muscles in response to supramaximal stimuli delivered to the ulnar nerve at the elbow. Three fatig...

The Journal of Physiology, 2011

Motor units serve both as the mechanical apparatus and the final stage of neural processing thr... more Motor units serve both as the mechanical apparatus and the final stage of neural processing through which motor behaviours are enacted. Therefore, knowledge about the contractile properties and organization of the neural inputs to motor units supplying finger muscles is essential for understanding the control strategies underlying the diverse motor functions of the human hand. In this brief review, basic contractile properties of motor units residing in human hand muscles are described. Hand motor units are not readily categorized into the classical physiological types as established in the cat gastrocnemius muscle. In addition, the distribution of descending synaptic inputs to motor nuclei supplying different hand muscles is outlined. Motor neurons innervating intrinsic muscles appear to have relatively independent lines of input from supraspinal centres whereas substantial divergence of descending input is seen across motor nuclei supplying extrinsic hand muscles. The functional...

The Journal of Neuroscience, 2005

Short-term synchrony was measured for pairs of motor units located within and across muscles acti... more Short-term synchrony was measured for pairs of motor units located within and across muscles activated during a task that mimicked precision grip in the dominant and nondominant hands of human subjects. Surprisingly, synchrony for pairs of motor units residing in separate muscles (flexor pollicis longus, a thumb muscle, and flexor digitorum profundus, an index-finger muscle) was just as large as that for pairs of units both within the thumb muscle. Furthermore, the high level of synchrony seen across muscles in the dominant hand was absent in the nondominant hand. These results suggest that descending pathways diverge to provide extensive common input across motor nuclei involved in the precision grip and that such divergence might contribute to the preferred use of one hand over the other.

Physiology & Behavior, 2008

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psyc... more The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans were stimulated successfully in the rhesus macaque and caused similar appearance changes to human facial movements. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from that of monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.