Eilon Vaadia | Hebrew Univesity of Jerusalem (original) (raw)

Papers by Eilon Vaadia

Research paper thumbnail of Learning about the learning-Brain:  mutual learning of brain and Machine in adaptive BMI settings

Frontiers in Neuroscience, 2010

Research paper thumbnail of The Representation of Visual and Motor Aspects of Reaching Movements in the Human Motor Cortex

The Journal of Neuroscience, Aug 24, 2011

Research paper thumbnail of Decision letter: Stretching the skin immediately enhances perceived stiffness and gradually enhances the predictive control of grip force

Research paper thumbnail of Decision letter: Stretching the skin immediately enhances perceived stiffness and gradually enhances the predictive control of grip force

Research paper thumbnail of Population subspaces reflect movement intention for arm and brain-machine interface control

Motor cortex is active during covert motor acts, such as action observation and mental rehearsal,... more Motor cortex is active during covert motor acts, such as action observation and mental rehearsal, when muscles are quiescent. Such neuronal activity, which is thought to be similar to the activity underlying overt movement, is exploited by neural prosthetics to afford subjects control of an external effector. We compared neural activity in primary motor cortex of monkeys who controlled a cursor using either their arm or a brain-machine interface (BMI) to identify what features of neural activity are similar or dissimilar in these two control contexts. Neuronal population activity parcellates into orthogonal subspaces, with some representations that are unique to arm movements and others that are shared between arm and BMI control. The shared subspace is invariant to the effector used and to biomechanical details of the movement, revealing a representation that reflects movement intention. This intention representation is likely the signal extracted by BMI algorithms for cursor contr...

Research paper thumbnail of Faculty of 1000 evaluation for Premotor and Motor Cortices Encode Reward

F1000 - Post-publication peer review of the biomedical literature, 2016

Rewards associated with actions are critical for motivation and learning about the consequences o... more Rewards associated with actions are critical for motivation and learning about the consequences of one's actions on the world. The motor cortices are involved in planning and executing movements, but it is unclear whether they encode reward over and above limb kinematics and dynamics. Here, we report a categorical reward signal in dorsal premotor (PMd) and primary motor (M1) neurons that corresponds to an increase in firing rates when a trial was not rewarded regardless of whether or not a reward was expected. We show that this signal is unrelated to error magnitude, reward prediction error, or other task confounds such as reward consumption, return reach plan, or kinematic differences across rewarded and unrewarded trials. The availability of reward information in motor cortex is crucial for theories of reward-based learning and motivational influences on actions.

Research paper thumbnail of Abstracts of the 16th Annual Meeting of The Israel Society for Neuroscience: Eilat, Israel, November 25–27, 2007

Neural Plasticity, 2007

The Israel Society for Neuroscience—ISFN—was founded in 1993 by a group of Israeli leading scient... more The Israel Society for Neuroscience—ISFN—was founded in 1993 by a group of Israeli leading scientists conducting research in the area of neurobiology. The primary goal of the society was to promote and disseminate the knowledge and understanding acquired by its members, and to strengthen interactions between them. Since then, the society holds its annual meeting every year in Eilat usually during December. At this annual meetings, the senior Israeli neurobiologists, their teams, and their graduate students, as well as foreign scientists and students, present their recent research findings in platform and poster presentations, and the program of the meeting is mainly based on the 338 received abstracts which are published in this volume. The meeting also offers the opportunity for the researchers to exchange information with each other, often leading to the initiation of collaborative studies. Both the number of members of the society and those participating in the annual meeting is ...

Research paper thumbnail of Phase-specific microstimulation in brain machine interface setting differentially modulates beta oscillations and affects behavior

It is widely accepted that beta-band oscillations play a role in sensorimotor behavior. To furthe... more It is widely accepted that beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a novel hybrid platform to combine operant conditioning and phasespecific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrodes arrays in motor cortex, to volitionally enhance local field potential (LFP) beta-band (20-30Hz) activity at selected sites using a brain-machine interface (BMI). We demonstrate that beta oscillations of LFP and single-unit spiking activity increased dramatically with BMI training, and that pre-movement Beta-power was anti-correlated with task performance. We also show that phase-specific ICMS modulated the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induced phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling of the functional role of cortical oscillations, and to future development of clinical tools for ameliorating abnormal neuronal activities in brain diseases.

Research paper thumbnail of Speculations on a Neural Substrate for Immediate Memory

Springer eBooks, 1975

We carry with us a fairly detailed memory of the immediate past. In the course of time, a huge bu... more We carry with us a fairly detailed memory of the immediate past. In the course of time, a huge bulk of information passes through this memory, but only a fraction remains available for long periods. It is generally accepted that the memory of the near past is carried by the electric activity of the cerebral nerve cells. This assumption is based mainly on two arguments: (a) It is hard to conceive of any mechanism whereby stored information could be continuously modified to encompass an endless spectrum of variations except by electrical activity. (b) Any major disturbance of the electrical activity of the brain (such as electro-shock, hypoglycemic shock or concussion) disrupts the memory of events preceding the disturbance.

Research paper thumbnail of Temporal firing patterns of single units, pairs and triplets of units in the auditory cortex

PubMed, 1987

The spontaneous and acoustically driven activities of single units, pairs and triplets of units i... more The spontaneous and acoustically driven activities of single units, pairs and triplets of units in the auditory cortex were analyzed. Data were obtained in two sets of experiments from nonbehaving awake cats and from a behaving monkey. The results of the two sets of experiments indicated that neighboring neurons usually fire independently. The weak correlations found between pairs of adjacent neurons were mostly indicative of a common input driving both units. In some cases, signs of synaptic interaction between the neurons were found. When triplets of units were considered, it was found that several independent inputs exist, even within a small group of adjacent neurons. When such small groups of neurons were studied in the behaving monkey, it was found that the temporal firing pattern of single neurons and the interactions between pairs of neurons were in some cases dependent on the behavioral state and on the sensorimotor association.

Research paper thumbnail of Differences in Context and Feedback Result in Different Trajectories and Adaptation Strategies in Reaching

PLOS ONE, Jan 16, 2009

Computational models of motor control have often explained the straightness of horizontal planar ... more Computational models of motor control have often explained the straightness of horizontal planar reaching movements as a consequence of optimal control. Departure from rectilinearity is thus regarded as sub-optimal. Here we examine if subjects may instead select to make curved trajectories following adaptation to force fields and visuomotor rotations. Separate subjects adapted to force fields with or without visual feedback of their hand trajectory and were retested after 24 hours. Following adaptation, comparable accuracies were achieved in two ways: with visual feedback, adapted trajectories in force fields were straight whereas without it, they remained curved. The results suggest that trajectory shape is not always straight, but is also influenced by the calibration of available feedback signals for the state estimation required by the task. In a follow-up experiment, where additional subjects learned a visuomotor rotation immediately after force field, the trajectories learned in force fields (straight or curved) were transferred when directions of the perturbations were similar but not when directions were opposing. This demonstrates a strong bias by prior experience to keep using a recently acquired control policy that continues to produce successful performance inspite of differences in tasks and feedback conditions. On relearning of force fields on the second day, facilitation by intervening visuomotor rotations occurred only when required motor adjustments and calibration of feedback signals were similar in both tasks. These results suggest that both the available feedback signals and prior history of learning influence the choice and maintenance of control policy during adaptations.

Research paper thumbnail of The Neuronal Basis of Long-Term Sensorimotor Learning

The Journal of Neuroscience, Jan 5, 2011

The brain has a remarkable ability to learn and adjust behavior. For instance, the brain can adju... more The brain has a remarkable ability to learn and adjust behavior. For instance, the brain can adjust muscle activation to cope with changes in the environment. However, the neuronal mechanisms behind this adaptation are not clear. To address this fundamental question, this study examines the neuronal basis of long-term sensorimotor learning by recording neuronal activity in the primary motor cortex of monkeys during a long-term adaptation to a force-field perturbation. For 5 consecutive days, the same perturbation was applied to the monkey's hand when reaching to a single target, whereas movements to all other targets were not perturbed. The gradual improvement in performance over these 5 days was correlated to the evolvement in the population neuronal signal, with two timescales of changes in single-cell activity. Specifically, one subgroup of cells showed a relatively fast increase in activity, whereas the other showed a gradual, slower decrease. These adapted patterns of neuronal activity did not involve changes in directional tuning of single cells, suggesting that adaptation was the result of adjustments of the required motor plan by a population of neurons rather than changes in single-cell properties. Furthermore, generalization was mostly expressed in the direction of the required compensatory force during adaptation. Altogether, the neuronal activity and its generalization accord with the adapted motor plan.

Research paper thumbnail of Emergence of Novel Representations in Primary Motor Cortex and Premotor Neurons during Associative Learning

The Journal of Neuroscience, Sep 17, 2008

Neurons in the motor areas of cortex play a key role in associating sensory instructions with mov... more Neurons in the motor areas of cortex play a key role in associating sensory instructions with movements. However, their ability to acquire and maintain representations of novel stimulus features, especially when these features are behaviorally relevant, remains unknown. We investigated neuronal changes in these areas during and after associative learning, by training monkeys on a novel reaching task that required associating target colors with movement directions. Before and after learning, the monkeys performed a well known center-out task. We found that during learning, up to 48% of the neurons developed learning-related responses, differentiating between the associative task and the center-out task, although movement kinematics were the same. After learning, on returning to the center-out task in which color was irrelevant, many of these neurons maintained their response to the associative task; they displayed novel sensitivity to the color of the target that was relevant during learning. These neuronal responses prevailed in both the primary motor cortex and the ventral and dorsal premotor cortices, without degrading the information that the neurons firing carried about movement direction. Our results show that motor cortical neurons can rapidly develop and maintain sensitivities to novel arbitrary sensory features such as color, when such features are behaviorally relevant.

Research paper thumbnail of In search of the best stimulus: An optimization procedure for finding efficient stimuli in the cat auditory cortex

Hearing Research, 1994

Units in the auditory cortex of cats respond to a large variety of stimuli: pure tones, AM-and FM... more Units in the auditory cortex of cats respond to a large variety of stimuli: pure tones, AM-and FM-modulated signals, clicks, wideband noise, natural sounds, and more. However, no single family of sounds was found to be optimal (in the sense that oriented lines are optimal in the visual cortex). The search for optimal complex sounds is hard because of the high dimensionality of the space of interesting sounds. In an effort to overcome this problem, an automatic search procedure for finding efficient stimuli in high-dimensional sound spaces was developed. This procedure chooses the stimuli to be presented according to the responses to past stimuli, trying to increase the strength of the response. The results of applying this method to recordings of population activity in the primary auditory cortex of cats are described. The search was applied to single tones. two-tone stimuli, four-tone stimuli and to a two-dimensional subset of nine-tone stimuli, parametrized by the center frequency and the fixed difference between adjacent frequencies. The method was able to find efficient stimuli, and its performance improved with the dimension of the sound spaces. Efficient stimuli, found in different optimization runs using population activity recorded from the same electrode, often shared similar frequencies and pairs of frequencies, and tended to evoke similar levels of activity. This result indicates that a global analysis of the location of spectral peaks is performed at the level of the auditory cortex.

Research paper thumbnail of Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements

European Journal of Neuroscience, Dec 1, 2001

Cortico-cortical connections through the corpus callosum are a major candidate for mediating bima... more Cortico-cortical connections through the corpus callosum are a major candidate for mediating bimanual coordination. However, aside from the de®cits observed after lesioning this connection, little positive evidence indicates its function in bimanual tasks. In order to address this issue, we simultaneously recorded neuronal activity at multiple sites within the arm area of motor cortex in both hemispheres of awake primates performing different bimanual and unimanual movements. By employing an adapted form of the joint peri-stimulus time histogram technique, we discovered rapid movement-related correlation changes between the local ®eld potentials (LFPs) of the two hemispheres that escaped detection by time-averaged cross-correlation methods. The frequency and amplitude of dynamic modi®cations in correlations between the hemispheres were similar to those within the same hemisphere. As in previous EEG studies, we found that, on average, correlation decreased during movements. However, a subset of recording site pairs did show transiently increased correlations around movement onset (57% of all pairs and conditions in monkey G, 39% in monkey P). In interhemispheric pairs, these increases were consistently related to the mode of coupling between the two arms. Both the correlations between the movements themselves and the interhemispheric LFP correlation increases were strongest during bimanual symmetric movements, and weaker during bimanual asymmetric and unimanual movements. Increased correlations occurred mainly around movement onset, whilst decreases in correlation dominated during movement execution. The task-speci®c way in which interhemispheric correlations are modulated is compatible with the notion that interactions between the hemispheres contribute to behavioural coupling between the arms.

Research paper thumbnail of Inducing Gamma Oscillations and Precise Spike Synchrony by Operant Conditioning via Brain-Machine Interface

Neuron, 2013

Neural oscillations in the low-gamma range (30-50 Hz) have been implicated in neuronal synchrony,... more Neural oscillations in the low-gamma range (30-50 Hz) have been implicated in neuronal synchrony, computation, behavior, and cognition. Abnormal low-gamma activity, hypothesized to reflect impaired synchronization, has been evidenced in several brain disorders. Thus, understanding the relations between gamma oscillations, neuronal synchrony and behavior is a major research challenge. We used a brain-machine interface (BMI) to train monkeys to specifically increase low-gamma power in selected sites of motor cortex to move a cursor and obtain a reward. The monkeys learned to robustly generate oscillatory gamma waves, which were accompanied by a dramatic increase of spiking synchrony of highly precise spatiotemporal patterns. The findings link volitional control of LFP oscillations, neuronal synchrony, and the behavioral outcome. Subjects' ability to directly modulate specific patterns of neuronal synchrony provides a powerful approach for understanding neuronal processing in relation to behavior and for the use of BMIs in a clinical setting. Neuron Inducing g-LFP Oscillations and Spike Synchrony

Research paper thumbnail of Relationship between single-unit activity, local and surface electro-cortico-gram demonstrate dynamic organization of cell population in the cortex

Behavioural Brain Research, Apr 1, 1986

Research paper thumbnail of Phase-Specific Microstimulation Differentially Modulates Beta Oscillations and Affects Behavior

Cell Reports, Feb 1, 2020

It is widely accepted that Beta-band oscillations play a role in sensorimotor behavior. To furthe... more It is widely accepted that Beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a hybrid platform to combine neural operant conditioning and phase-specific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrode arrays in the motor cortex, to volitionally enhance local field potential (LFP) Beta-band (20-30 Hz) activity at selected sites using a brain-machine interface. We find that Beta oscillations of LFP and single-unit spiking activity increase dramatically with brain-machine interface training and that pre-movement Beta power is anti-correlated with task performance. We also find that phase-specific ICMS modulates the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induces phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling the functional role of cortical oscillations and to the future development of clinical tools for ameliorating abnormal neuronal activities in brain disease.

Research paper thumbnail of Neuronal Correlates of Memory Formation in Motor Cortex after Adaptation to Force Field

The Journal of Neuroscience, Jul 7, 2010

Activity of single neurons in the motor cortex has been shown to change during acquisition of mot... more Activity of single neurons in the motor cortex has been shown to change during acquisition of motor skills. We previously reported that the combined activity of cell ensembles in the motor cortex of monkeys (Macaca fascicularis) evolves during adaptation to a novel force field perturbation to encode the direction of compensatory force when reaching to visual targets. We also showed that the population directional signal was altered by the available sensory feedback. Here, we examined whether traces of such activity would linger on to later constitute motor memories of the newly acquired skill and whether memory traces would differ depending on feedback. We found that motor-cortical cell ensembles retained features of their adaptive activity pattern in the absence of perturbation when reaching to both learned and unlearned targets. Moreover, the preferred directions of these cells rotated in the direction of force field while the entire population of cells produced no net rotation of preferred direction when returning to null-field reaches. Whereas the activity pattern and preferred direction rotations were comparable with and without visual feedback, changes in tuning amplitudes differed across feedback conditions. Last, savings in behavioral performance and neuronal activity during later reexposure to force field were apparent. Overall, the findings reflect a novel representation of motor memory by cell ensembles and indicate a putative role of the motor cortex in early acquisition of motor memory.

Research paper thumbnail of Neuronal activities related to higher brain functions-theoretical and experimental implications

IEEE Transactions on Biomedical Engineering, 1989

The activities of several single units (6-10) were recorded simultaneously in the auditory cortex... more The activities of several single units (6-10) were recorded simultaneously in the auditory cortex and in frontal cortical areas of cats and monkeys. The response properties of the single units and the interaction between them were studied. It is shown that single units in both areas may participate in prolonged processes and he involved in more than one process. Adjacent neurons need not function in unison; while some neurons are activated, others may stay inactive. The interactions among adjacent neurons are weak, and can be modulated by sensory stimulation, and by arousal and behavioral states. These properties lead us to hypothesize that information is represented in the cortex by coactivation of sets of neurons rather than by independent modulation of the single-unit firing rate. A single unit may be a member of several representing sets. Thus, each neuron may participate in more than one function and each small cortical area may contain members of several functional sets. A mechanism for computing and transmitting information, based on converging-diverging links, between neuronal sets is described and tested by simulations and analysis of experimental data.

Research paper thumbnail of Learning about the learning-Brain:  mutual learning of brain and Machine in adaptive BMI settings

Frontiers in Neuroscience, 2010

Research paper thumbnail of The Representation of Visual and Motor Aspects of Reaching Movements in the Human Motor Cortex

The Journal of Neuroscience, Aug 24, 2011

Research paper thumbnail of Decision letter: Stretching the skin immediately enhances perceived stiffness and gradually enhances the predictive control of grip force

Research paper thumbnail of Decision letter: Stretching the skin immediately enhances perceived stiffness and gradually enhances the predictive control of grip force

Research paper thumbnail of Population subspaces reflect movement intention for arm and brain-machine interface control

Motor cortex is active during covert motor acts, such as action observation and mental rehearsal,... more Motor cortex is active during covert motor acts, such as action observation and mental rehearsal, when muscles are quiescent. Such neuronal activity, which is thought to be similar to the activity underlying overt movement, is exploited by neural prosthetics to afford subjects control of an external effector. We compared neural activity in primary motor cortex of monkeys who controlled a cursor using either their arm or a brain-machine interface (BMI) to identify what features of neural activity are similar or dissimilar in these two control contexts. Neuronal population activity parcellates into orthogonal subspaces, with some representations that are unique to arm movements and others that are shared between arm and BMI control. The shared subspace is invariant to the effector used and to biomechanical details of the movement, revealing a representation that reflects movement intention. This intention representation is likely the signal extracted by BMI algorithms for cursor contr...

Research paper thumbnail of Faculty of 1000 evaluation for Premotor and Motor Cortices Encode Reward

F1000 - Post-publication peer review of the biomedical literature, 2016

Rewards associated with actions are critical for motivation and learning about the consequences o... more Rewards associated with actions are critical for motivation and learning about the consequences of one's actions on the world. The motor cortices are involved in planning and executing movements, but it is unclear whether they encode reward over and above limb kinematics and dynamics. Here, we report a categorical reward signal in dorsal premotor (PMd) and primary motor (M1) neurons that corresponds to an increase in firing rates when a trial was not rewarded regardless of whether or not a reward was expected. We show that this signal is unrelated to error magnitude, reward prediction error, or other task confounds such as reward consumption, return reach plan, or kinematic differences across rewarded and unrewarded trials. The availability of reward information in motor cortex is crucial for theories of reward-based learning and motivational influences on actions.

Research paper thumbnail of Abstracts of the 16th Annual Meeting of The Israel Society for Neuroscience: Eilat, Israel, November 25–27, 2007

Neural Plasticity, 2007

The Israel Society for Neuroscience—ISFN—was founded in 1993 by a group of Israeli leading scient... more The Israel Society for Neuroscience—ISFN—was founded in 1993 by a group of Israeli leading scientists conducting research in the area of neurobiology. The primary goal of the society was to promote and disseminate the knowledge and understanding acquired by its members, and to strengthen interactions between them. Since then, the society holds its annual meeting every year in Eilat usually during December. At this annual meetings, the senior Israeli neurobiologists, their teams, and their graduate students, as well as foreign scientists and students, present their recent research findings in platform and poster presentations, and the program of the meeting is mainly based on the 338 received abstracts which are published in this volume. The meeting also offers the opportunity for the researchers to exchange information with each other, often leading to the initiation of collaborative studies. Both the number of members of the society and those participating in the annual meeting is ...

Research paper thumbnail of Phase-specific microstimulation in brain machine interface setting differentially modulates beta oscillations and affects behavior

It is widely accepted that beta-band oscillations play a role in sensorimotor behavior. To furthe... more It is widely accepted that beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a novel hybrid platform to combine operant conditioning and phasespecific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrodes arrays in motor cortex, to volitionally enhance local field potential (LFP) beta-band (20-30Hz) activity at selected sites using a brain-machine interface (BMI). We demonstrate that beta oscillations of LFP and single-unit spiking activity increased dramatically with BMI training, and that pre-movement Beta-power was anti-correlated with task performance. We also show that phase-specific ICMS modulated the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induced phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling of the functional role of cortical oscillations, and to future development of clinical tools for ameliorating abnormal neuronal activities in brain diseases.

Research paper thumbnail of Speculations on a Neural Substrate for Immediate Memory

Springer eBooks, 1975

We carry with us a fairly detailed memory of the immediate past. In the course of time, a huge bu... more We carry with us a fairly detailed memory of the immediate past. In the course of time, a huge bulk of information passes through this memory, but only a fraction remains available for long periods. It is generally accepted that the memory of the near past is carried by the electric activity of the cerebral nerve cells. This assumption is based mainly on two arguments: (a) It is hard to conceive of any mechanism whereby stored information could be continuously modified to encompass an endless spectrum of variations except by electrical activity. (b) Any major disturbance of the electrical activity of the brain (such as electro-shock, hypoglycemic shock or concussion) disrupts the memory of events preceding the disturbance.

Research paper thumbnail of Temporal firing patterns of single units, pairs and triplets of units in the auditory cortex

PubMed, 1987

The spontaneous and acoustically driven activities of single units, pairs and triplets of units i... more The spontaneous and acoustically driven activities of single units, pairs and triplets of units in the auditory cortex were analyzed. Data were obtained in two sets of experiments from nonbehaving awake cats and from a behaving monkey. The results of the two sets of experiments indicated that neighboring neurons usually fire independently. The weak correlations found between pairs of adjacent neurons were mostly indicative of a common input driving both units. In some cases, signs of synaptic interaction between the neurons were found. When triplets of units were considered, it was found that several independent inputs exist, even within a small group of adjacent neurons. When such small groups of neurons were studied in the behaving monkey, it was found that the temporal firing pattern of single neurons and the interactions between pairs of neurons were in some cases dependent on the behavioral state and on the sensorimotor association.

Research paper thumbnail of Differences in Context and Feedback Result in Different Trajectories and Adaptation Strategies in Reaching

PLOS ONE, Jan 16, 2009

Computational models of motor control have often explained the straightness of horizontal planar ... more Computational models of motor control have often explained the straightness of horizontal planar reaching movements as a consequence of optimal control. Departure from rectilinearity is thus regarded as sub-optimal. Here we examine if subjects may instead select to make curved trajectories following adaptation to force fields and visuomotor rotations. Separate subjects adapted to force fields with or without visual feedback of their hand trajectory and were retested after 24 hours. Following adaptation, comparable accuracies were achieved in two ways: with visual feedback, adapted trajectories in force fields were straight whereas without it, they remained curved. The results suggest that trajectory shape is not always straight, but is also influenced by the calibration of available feedback signals for the state estimation required by the task. In a follow-up experiment, where additional subjects learned a visuomotor rotation immediately after force field, the trajectories learned in force fields (straight or curved) were transferred when directions of the perturbations were similar but not when directions were opposing. This demonstrates a strong bias by prior experience to keep using a recently acquired control policy that continues to produce successful performance inspite of differences in tasks and feedback conditions. On relearning of force fields on the second day, facilitation by intervening visuomotor rotations occurred only when required motor adjustments and calibration of feedback signals were similar in both tasks. These results suggest that both the available feedback signals and prior history of learning influence the choice and maintenance of control policy during adaptations.

Research paper thumbnail of The Neuronal Basis of Long-Term Sensorimotor Learning

The Journal of Neuroscience, Jan 5, 2011

The brain has a remarkable ability to learn and adjust behavior. For instance, the brain can adju... more The brain has a remarkable ability to learn and adjust behavior. For instance, the brain can adjust muscle activation to cope with changes in the environment. However, the neuronal mechanisms behind this adaptation are not clear. To address this fundamental question, this study examines the neuronal basis of long-term sensorimotor learning by recording neuronal activity in the primary motor cortex of monkeys during a long-term adaptation to a force-field perturbation. For 5 consecutive days, the same perturbation was applied to the monkey's hand when reaching to a single target, whereas movements to all other targets were not perturbed. The gradual improvement in performance over these 5 days was correlated to the evolvement in the population neuronal signal, with two timescales of changes in single-cell activity. Specifically, one subgroup of cells showed a relatively fast increase in activity, whereas the other showed a gradual, slower decrease. These adapted patterns of neuronal activity did not involve changes in directional tuning of single cells, suggesting that adaptation was the result of adjustments of the required motor plan by a population of neurons rather than changes in single-cell properties. Furthermore, generalization was mostly expressed in the direction of the required compensatory force during adaptation. Altogether, the neuronal activity and its generalization accord with the adapted motor plan.

Research paper thumbnail of Emergence of Novel Representations in Primary Motor Cortex and Premotor Neurons during Associative Learning

The Journal of Neuroscience, Sep 17, 2008

Neurons in the motor areas of cortex play a key role in associating sensory instructions with mov... more Neurons in the motor areas of cortex play a key role in associating sensory instructions with movements. However, their ability to acquire and maintain representations of novel stimulus features, especially when these features are behaviorally relevant, remains unknown. We investigated neuronal changes in these areas during and after associative learning, by training monkeys on a novel reaching task that required associating target colors with movement directions. Before and after learning, the monkeys performed a well known center-out task. We found that during learning, up to 48% of the neurons developed learning-related responses, differentiating between the associative task and the center-out task, although movement kinematics were the same. After learning, on returning to the center-out task in which color was irrelevant, many of these neurons maintained their response to the associative task; they displayed novel sensitivity to the color of the target that was relevant during learning. These neuronal responses prevailed in both the primary motor cortex and the ventral and dorsal premotor cortices, without degrading the information that the neurons firing carried about movement direction. Our results show that motor cortical neurons can rapidly develop and maintain sensitivities to novel arbitrary sensory features such as color, when such features are behaviorally relevant.

Research paper thumbnail of In search of the best stimulus: An optimization procedure for finding efficient stimuli in the cat auditory cortex

Hearing Research, 1994

Units in the auditory cortex of cats respond to a large variety of stimuli: pure tones, AM-and FM... more Units in the auditory cortex of cats respond to a large variety of stimuli: pure tones, AM-and FM-modulated signals, clicks, wideband noise, natural sounds, and more. However, no single family of sounds was found to be optimal (in the sense that oriented lines are optimal in the visual cortex). The search for optimal complex sounds is hard because of the high dimensionality of the space of interesting sounds. In an effort to overcome this problem, an automatic search procedure for finding efficient stimuli in high-dimensional sound spaces was developed. This procedure chooses the stimuli to be presented according to the responses to past stimuli, trying to increase the strength of the response. The results of applying this method to recordings of population activity in the primary auditory cortex of cats are described. The search was applied to single tones. two-tone stimuli, four-tone stimuli and to a two-dimensional subset of nine-tone stimuli, parametrized by the center frequency and the fixed difference between adjacent frequencies. The method was able to find efficient stimuli, and its performance improved with the dimension of the sound spaces. Efficient stimuli, found in different optimization runs using population activity recorded from the same electrode, often shared similar frequencies and pairs of frequencies, and tended to evoke similar levels of activity. This result indicates that a global analysis of the location of spectral peaks is performed at the level of the auditory cortex.

Research paper thumbnail of Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements

European Journal of Neuroscience, Dec 1, 2001

Cortico-cortical connections through the corpus callosum are a major candidate for mediating bima... more Cortico-cortical connections through the corpus callosum are a major candidate for mediating bimanual coordination. However, aside from the de®cits observed after lesioning this connection, little positive evidence indicates its function in bimanual tasks. In order to address this issue, we simultaneously recorded neuronal activity at multiple sites within the arm area of motor cortex in both hemispheres of awake primates performing different bimanual and unimanual movements. By employing an adapted form of the joint peri-stimulus time histogram technique, we discovered rapid movement-related correlation changes between the local ®eld potentials (LFPs) of the two hemispheres that escaped detection by time-averaged cross-correlation methods. The frequency and amplitude of dynamic modi®cations in correlations between the hemispheres were similar to those within the same hemisphere. As in previous EEG studies, we found that, on average, correlation decreased during movements. However, a subset of recording site pairs did show transiently increased correlations around movement onset (57% of all pairs and conditions in monkey G, 39% in monkey P). In interhemispheric pairs, these increases were consistently related to the mode of coupling between the two arms. Both the correlations between the movements themselves and the interhemispheric LFP correlation increases were strongest during bimanual symmetric movements, and weaker during bimanual asymmetric and unimanual movements. Increased correlations occurred mainly around movement onset, whilst decreases in correlation dominated during movement execution. The task-speci®c way in which interhemispheric correlations are modulated is compatible with the notion that interactions between the hemispheres contribute to behavioural coupling between the arms.

Research paper thumbnail of Inducing Gamma Oscillations and Precise Spike Synchrony by Operant Conditioning via Brain-Machine Interface

Neuron, 2013

Neural oscillations in the low-gamma range (30-50 Hz) have been implicated in neuronal synchrony,... more Neural oscillations in the low-gamma range (30-50 Hz) have been implicated in neuronal synchrony, computation, behavior, and cognition. Abnormal low-gamma activity, hypothesized to reflect impaired synchronization, has been evidenced in several brain disorders. Thus, understanding the relations between gamma oscillations, neuronal synchrony and behavior is a major research challenge. We used a brain-machine interface (BMI) to train monkeys to specifically increase low-gamma power in selected sites of motor cortex to move a cursor and obtain a reward. The monkeys learned to robustly generate oscillatory gamma waves, which were accompanied by a dramatic increase of spiking synchrony of highly precise spatiotemporal patterns. The findings link volitional control of LFP oscillations, neuronal synchrony, and the behavioral outcome. Subjects' ability to directly modulate specific patterns of neuronal synchrony provides a powerful approach for understanding neuronal processing in relation to behavior and for the use of BMIs in a clinical setting. Neuron Inducing g-LFP Oscillations and Spike Synchrony

Research paper thumbnail of Relationship between single-unit activity, local and surface electro-cortico-gram demonstrate dynamic organization of cell population in the cortex

Behavioural Brain Research, Apr 1, 1986

Research paper thumbnail of Phase-Specific Microstimulation Differentially Modulates Beta Oscillations and Affects Behavior

Cell Reports, Feb 1, 2020

It is widely accepted that Beta-band oscillations play a role in sensorimotor behavior. To furthe... more It is widely accepted that Beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a hybrid platform to combine neural operant conditioning and phase-specific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrode arrays in the motor cortex, to volitionally enhance local field potential (LFP) Beta-band (20-30 Hz) activity at selected sites using a brain-machine interface. We find that Beta oscillations of LFP and single-unit spiking activity increase dramatically with brain-machine interface training and that pre-movement Beta power is anti-correlated with task performance. We also find that phase-specific ICMS modulates the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induces phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling the functional role of cortical oscillations and to the future development of clinical tools for ameliorating abnormal neuronal activities in brain disease.

Research paper thumbnail of Neuronal Correlates of Memory Formation in Motor Cortex after Adaptation to Force Field

The Journal of Neuroscience, Jul 7, 2010

Activity of single neurons in the motor cortex has been shown to change during acquisition of mot... more Activity of single neurons in the motor cortex has been shown to change during acquisition of motor skills. We previously reported that the combined activity of cell ensembles in the motor cortex of monkeys (Macaca fascicularis) evolves during adaptation to a novel force field perturbation to encode the direction of compensatory force when reaching to visual targets. We also showed that the population directional signal was altered by the available sensory feedback. Here, we examined whether traces of such activity would linger on to later constitute motor memories of the newly acquired skill and whether memory traces would differ depending on feedback. We found that motor-cortical cell ensembles retained features of their adaptive activity pattern in the absence of perturbation when reaching to both learned and unlearned targets. Moreover, the preferred directions of these cells rotated in the direction of force field while the entire population of cells produced no net rotation of preferred direction when returning to null-field reaches. Whereas the activity pattern and preferred direction rotations were comparable with and without visual feedback, changes in tuning amplitudes differed across feedback conditions. Last, savings in behavioral performance and neuronal activity during later reexposure to force field were apparent. Overall, the findings reflect a novel representation of motor memory by cell ensembles and indicate a putative role of the motor cortex in early acquisition of motor memory.

Research paper thumbnail of Neuronal activities related to higher brain functions-theoretical and experimental implications

IEEE Transactions on Biomedical Engineering, 1989

The activities of several single units (6-10) were recorded simultaneously in the auditory cortex... more The activities of several single units (6-10) were recorded simultaneously in the auditory cortex and in frontal cortical areas of cats and monkeys. The response properties of the single units and the interaction between them were studied. It is shown that single units in both areas may participate in prolonged processes and he involved in more than one process. Adjacent neurons need not function in unison; while some neurons are activated, others may stay inactive. The interactions among adjacent neurons are weak, and can be modulated by sensory stimulation, and by arousal and behavioral states. These properties lead us to hypothesize that information is represented in the cortex by coactivation of sets of neurons rather than by independent modulation of the single-unit firing rate. A single unit may be a member of several representing sets. Thus, each neuron may participate in more than one function and each small cortical area may contain members of several functional sets. A mechanism for computing and transmitting information, based on converging-diverging links, between neuronal sets is described and tested by simulations and analysis of experimental data.