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Realization of reaching and grasping movements by a paralytic person or an amputee would greatly facilitate her/his activities of daily living. Towards this goal, control of a computer cursor or robotic arm using neural signals has been demonstrated in rodents, non-human primates and humans. This technology is commonly referred to as a Brain-Machine Interface (BMI) and is achieved by predictions of kinematic parameters, e.g. position or velocity. However, execution of natural movements, such as swinging baseball bats of different weights at the same speed, requires advanced planning for necessary context-specific forces in addition to kinematic control. Here we show, for the first time, the control of a virtual arm with representative inertial parameters using real-time neural control of torques in non-human primates (M. radiata). We found that neural control of torques leads to ballistic, possibly more naturalistic movements than position control alone, and that adding the influence of position in a hybrid torque-position control changes the feedforward behavior of these BMI movements. In addition, this level of control was achievable utilizing the neural recordings from either contralateral or ipsilateral M1. We also observed changed behavior of hybrid torque-position control under novel external dynamic environments that was comparable to natural movements. Our results demonstrate that inclusion of torque control to drive a neuroprosthetic device gives the user a more direct handle on the movement execution, especially when dealing with novel or changing dynamic environments. We anticipate our results to be a starting point of more sophisticated algorithms for sensorimotor neuroprostheses, eliminating the need of fully automatic kinematic-to-dynamic transformations as currently used by traditional kinematic-based decoders. Thus, we propose that direct control of torques, or other force related variables, should allow for more natural neuroprosthetic movements by the user.

Decision-making ability in the frontal lobe (among other brain structures) relies on the assignment of value to states of the animal and its environment. Then higher valued states can be pursued and lower (or negative) valued states avoided. The same principle forms the basis for computational reinforcement learning controllers, which have been fruitfully applied both as models of value estimation in the brain, and as artificial controllers in their own right. This work shows how state desirability signals decoded from frontal lobe hemodynamics, as measured with near-infrared spectroscopy (NIRS), can be applied as reinforcers to an adaptable artificial learning agent in order to guide its acquisition of skills. A set of experiments carried out on an alert macaque demonstrate that both oxy- and deoxyhemoglobin concentrations in the frontal lobe show differences in response to both primarily and secondarily desirable (versus undesirable) stimuli. This difference allows a NIRS signal classifier to serve successfully as a reinforcer for an adaptive controller performing a virtual tool-retrieval task. The agent's adaptability allows its performance to exceed the limits of the NIRS classifier decoding accuracy. We also show that decoding state desirabilities is more accurate when using relative concentrations of both oxyhemoglobin and deoxyhemoglobin, rather than either species alone.

Electrical stimulation of the nervous system for therapeutic purposes, such as deep brain stimulation in the treatment of Parkinson's disease, has been used for decades. Recently, increased attention has focused on using microstimulation to restore functions as diverse as somatosensation and memory. However, how microstimulation changes the neural substrate is still not fully understood. Microstimulation may cause cortical changes that could either compete with or complement natural neural processes, and could result in neuroplastic changes rendering the region dysfunctional or even epileptic. As part of our efforts to produce neuroprosthetic devices and to further study the effects of microstimulation on the cortex, we stimulated and recorded from microelectrode arrays in the hand area of the primary somatosensory cortex (area 1) in two awake macaque monkeys. We applied a simple neuroprosthetic microstimulation protocol to a pair of electrodes in the area 1 array, using either random pulses or pulses time-locked to the recorded spiking activity of a reference neuron. This setup was replicated using a computer model of the thalamocortical system, which consisted of 1980 spiking neurons distributed among six cortical layers and two thalamic nuclei. Experimentally, we found that spike-triggered microstimulation induced cortical plasticity, as shown by increased unit-pair mutual information, while random microstimulation did not. In addition, there was an increased response to touch following spike-triggered microstimulation, along with decreased neural variability. The computer model successfully reproduced both qualitative and quantitative aspects of the experimental findings. The physiological findings of this study suggest that even simple microstimulation protocols can be used to increase somatosensory information flow.

Neural activity in the primary motor cortex (M1) is known to correlate with movement related variables including kinematics and dynamics. Our recent work, which we believe is part of a paradigm shift in sensorimotor research, has shown that in addition to these movement related variables, activity in M1 and the primary somatosensory cortex (S1) are also modulated by context, such as value, during both active movement and movement observation. Here we expand on the investigation of reward modulation in M1, showing that reward level changes the neural tuning function of M1 units to both kinematic as well as dynamic related variables. In addition, we show that this reward-modulated activity is present during brain machine interface (BMI) control. We suggest that by taking into account these context dependencies of M1 modulation, we can produce more robust BMIs. Toward this goal, we demonstrate that we can classify reward expectation from M1 on a movement-by-movement basis under BMI control and use this to gate multiple linear BMI decoders toward improved offline performance. These findings demonstrate that it is possible and meaningful to design a more accurate BMI decoder that takes reward and context into consideration. Our next step in this development will be to incorporate this gating system, or a continuous variant of it, into online BMI performance.

Neural stimulation can be used as a tool to elicit natural sensations or behaviors by modulating neural activity. This can be potentially used to mitigate the damage of brain lesions or neural disorders. However, in order to obtain the optimal stimulation sequences, it is necessary to develop neural control methods, for example by constructing an inverse model of the target system. For real brains, this can be very challenging, and often unfeasible, as it requires repeatedly stimulating the neural system to obtain enough probing data, and depends on an unwarranted assumption of stationarity. By contrast, detailed brain simulations may provide an alternative testbed for understanding the interactions between ongoing neural activity and external stimulation. Unlike real brains, the artificial system can be probed extensively and precisely, and detailed output information is readily available. Here we employed a spiking network model of sensorimotor cortex trained to drive a realistic virtual musculoskeletal arm to reach a target. The network was then perturbed, in order to simulate a lesion, by either silencing neurons or removing synaptic connections. All lesions led to significant behvaioral impairments during the reaching task. The remaining cells were then systematically probed with a set of single and multiple-cell stimulations, and results were used to build an inverse model of the neural system. The inverse model was constructed using a kernel adaptive filtering method, and was used to predict the neural stimulation pattern required to recover the pre-lesion neural activity. Applying the derived neurostimulation to the lesioned network improved the reaching behavior performance. This work proposes a novel neurocontrol method, and provides theoretical groundwork on the use biomimetic brain models to develop and evaluate neurocontrollers that restore the function of damaged brain regions and the corresponding motor behaviors.

Embedding computational models in the physical world is a critical step towards constraining their behavior and building practical applications. Here we aim to drive a realistic musculoskeletal arm model using a biomimetic cortical spiking model, and make a robot arm reproduce the same trajectories in real time. Our cortical model consisted of a 3-layered cortex, composed of several hundred spiking model-neurons, which display physiologically realistic dynamics. We interconnected the cortical model to a two-joint musculoskeletal model of a human arm, with realistic anatomical and biomechanical properties. The virtual arm received muscle excitations from the neuronal model, and fed back proprioceptive information, forming a closed-loop system. The cortical model was trained using spike timing-dependent reinforcement learning to drive the virtual arm in a 2D reaching task. Limb position was used to simultaneously control a robot arm using an improved network interface. Virtual arm muscle activations responded to motoneuron firing rates, with virtual arm muscles lengths encoded via population coding in the proprioceptive population. After training, the virtual arm performed reaching movements which were smoother and more realistic than those obtained using a simplistic arm model. This system provided access to both spiking network properties and to arm biophysical properties, including muscle forces. The use of a musculoskeletal virtual arm and the improved control system allowed the robot arm to perform movements which were smoother than those reported in our previous paper using a simplistic arm. This work provides a novel approach consisting of bidirectionally connecting a cortical model to a realistic virtual arm, and using the system output to drive a robotic arm in real time. Our techniques are applicable to the future development of brain neuroprosthetic control systems, and may enable enhanced brain-machine interfaces with the possibility for finer control of limb prosthetics.

We study the feasibility and capability of the kernel temporal difference (KTD)(λ) algorithm for neural decoding. KTD(λ) is an online, kernel-based learning algorithm, which has been introduced to estimate value functions in reinforcement learning. This algorithm combines kernel-based representations with the temporal difference approach to learning. One of our key observations is that by using strictly positive definite kernels, algorithm’s convergence can be guaranteed for policy evaluation. The algorithm’s nonlinear functional approximation capabilities are shown in both simulations of policy evaluation and neural decoding problems (policy improvement). KTD can handle high-dimensional neural states containing spatial-temporal information at a reasonable computational complexity allowing real-time applications. When the algorithm seeks a proper mapping between a monkey’s neural states and desired positions of a computer cursor or a robot arm, in both open-loop and closed-loop experiments, it can effectively learn the neural state to action mapping. Finally, a visualization of the coadaptation process between the decoder and the subject shows the algorithm’s capabilities in reinforcement learning brain machine interfaces.

Brain machine interfaces (BMIs) have attracted intense attention as a promising technology for directly interfacing computers or prostheses with the brain’s motor and sensory areas, thereby bypassing the body. The availability of multiscale neural recordings including spike trains and local field potentials (LFPs) brings potential opportunities to enhance computational modeling by enriching the characterization of the neural system state. However, heterogeneity on data type (spike timing versus continuous amplitude signals) and spatiotemporal scale complicates the model integration of multiscale neural activity. In this paper, we propose a tensor-product-kernel-based framework to integrate the multiscale activity and exploit the complementary information available in multiscale neural activity. This provides a common mathematical framework for incorporating signals from different domains. The approach is applied to the problem of neural decoding and control. For neural decoding, the framework is able to identify the nonlinear functional relationship between the multiscale neural responses and the stimuli using general purpose kernel adaptive filtering. In a sensory stimulation experiment, the tensor-product-kernel decoder outperforms decoders that use only a single neural data type. In addition, an adaptive inverse controller for delivering electrical microstimulation patterns that utilizes the tensor-product kernel achieves promising results in emulating the responses to natural stimulation.

Previous studies have demonstrated changes in motor memories with the passage of time on the order of hours. We sought to further this work by determining the influence that time on the order of seconds has on motor learning by changing the duration between successive reaches (inter-reach-interval (IRI)). Human subjects made reaching movements to visual targets while holding onto a robotic manipulandum that presented a viscous curl field. We tested four experimental groups that differed with respect to the IRI (0.5, 5, 10 or 20 s). The 0.5 s IRI group performed significantly worse with respect to a learning index than the other groups over the first set of 192 reaches. Each group demonstrated significant learning during the first set. There was no significant difference with respect to the learning index between the 5, 10 and 20 s IRI groups. During the second and third set of 192 reaches the 0.5 s IRI group's performance became indistinguishable from the other groups indicating that with continued training the initial deficit in performance could be overcome.