Monkeys can learn to directly control the movements of an artificial actuator by using a brain-machine interface (BMI) driven by the activity of a sample of cortical neurons. Eventually, they can do so without moving their limbs. Neuronal adaptations underlying the transition from control of the limb to control of the actuator are poorly understood. Here, we show that rapid modifications in neuronal representation of velocity of the hand and actuator occur in multiple cortical areas during the operation of a BMI. Initially, monkeys controlled the actuator by moving a hand-held pole. During this period, the BMI was trained to predict the actuator velocity. As the monkeys started using their cortical activity to control the actuator, the activity of individual neurons and neuronal populations became less representative of the animal's hand movements while representing the movements of the actuator. As a result of this adaptation, the animals could eventually stop moving their hands yet continue to control the actuator. These results show that, during BMI control, cortical ensembles represent behaviorally significant motor parameters, even if these are not associated with movements of the animal's own limb.

The temporally encoded information obtained by vibrissal touch could be decoded "passively," involving only input-driven elements, or "actively," utilizing intrinsically driven oscillators. A previous study suggested that the trigeminal somatosensory system of rats does not obey the bottom-up order of activation predicted by passive decoding. Thus, we have tested whether this system obeys the predictions of active decoding. We have studied cortical single units in the somatosensory cortices of anesthetized rats and guinea pigs and found that about a quarter of them exhibit clear spontaneous oscillations, many of them around whisking frequencies (Ϸ10 Hz). The frequencies of these oscillations could be controlled locally by glutamate. These oscillations could be forced to track the frequency of induced rhythmic whisker movements at a stable, frequency-dependent, phase difference. During these stimulations, the response intensities of multiunits at the thalamic recipient layers of the cortex decreased, and their latencies increased, with increasing input frequency. These observations are consistent with thalamocortical loops implementing phase-locked loops, circuits that are most efficient in decoding temporally encoded information like that obtained by active vibrissal touch. According to this model, and consistent with our results, populations of thalamic "relay" neurons function as phase "comparators" that compare cortical timing expectations with the actual input timing and represent the difference by their population output rate.Rats, like other rodents, possess a specialized system for active touch. During tactile exploration, their whiskers scan the environment by rhythmic movements of 5-11 Hz (1, 2) to obtain sensory information about the location and texture of external objects (3, 4). Temporally, an object's location is encoded by the time interval between receptor firing at the onset of a whisking cycle and receptor firing due to perturbation of whisker motion by an external object [first-order vibrissal neurons respond strongly to these two events (5)]. This information could be decoded "passively;" that is, by feed-forward, bottom-up transformations utilizing neuronal temporal sensitivities (6) [axonal delay lines are not efficient at the millisecond range (7)]. Alternatively, temporal decoding could be obtained "actively," which involves top-down processes whereby intrinsic cortical oscillators track the input and provide a measure of its instantaneous frequency (8, 9).In passive decoding, sensory signals propagate in a feedforward manner to the cortex through thalamic "relay" neurons (Fig. 1A). Thus, whisker-locked activities of somatosensory thalamic neurons should lag brainstem but lead the cortical activities (Fig. 1B). In contrast, during whisker-locked oscillatory epochs in freely behaving rats, thalamic neurons phase-lag both brainstem and cortical neurons (10). Moreover, the oscillatory epochs are usually initiated at the cortex, further questioning the assumption of passive temporal d...

BackgroundDuring planning and execution of reaching movements, the activity of cortical motor neurons is modulated by a diversity of motor, sensory, and cognitive signals. Brain-machine interfaces (BMIs) extract part of these modulations to directly control artificial actuators. However, cortical modulations that emerge in the novel context of operating the BMI are poorly understood.Methodology/Principal FindingsHere we analyzed the changes in neuronal modulations that occurred in different cortical motor areas as monkeys learned to use a BMI to control reaching movements. Using spike-train analysis methods we demonstrate that the modulations of the firing-rates of cortical neurons increased abruptly after the monkeys started operating the BMI. Regression analysis revealed that these enhanced modulations were not correlated with the kinematics of the movement. The initial enhancement in firing rate modulations declined gradually with subsequent training in parallel with the improvement in behavioral performance.Conclusions/SignificanceWe conclude that the enhanced modulations are related to computational tasks that are significant especially in novel motor contexts. Although the function and neuronal mechanism of the enhanced cortical modulations are open for further inquiries, we discuss their potential role in processing execution errors and representing corrective or explorative activity. These representations are expected to contribute to the formation of internal models of the external actuator and their decoding may facilitate BMI improvement.

It has been proposed that animals and humans might choose a speed-accuracy tradeoff that maximizes reward rate. For this utility function the simple drift-diffusion model of two-alternative forced-choice tasks predicts a parameter-free optimal performance curve that relates normalized decision times to error rates under varying task conditions. However, behavioral data indicate that only ≈ 30% of subjects achieve optimality, and here we investigate the possibility that, in allowing for uncertainties, subjects might exercise robust strategies instead of optimal ones. We consider two strategies in which robustness is achieved by relinquishing performance: maximin and robust-satisficing. The former supposes maximization of guaranteed performance under a presumed level of uncertainty; the latter assumes that subjects require a critical performance level and maximize the level of uncertainty under which it can be guaranteed. These strategies respectively yield performance curves parameterized by presumed uncertainty level and required performance. Maximin performance curves for uncertainties in response-to-stimulus interval match data for the lower-scoring 70% of subjects well, and are more likely to explain it than robust-satisficing or alternative optimal performance curves that emphasize accuracy. For uncertainties in signal-to-noise ratio, neither maximin nor robust-satisficing performance curves adequately describe the data. We discuss implications for decisions under uncertainties, and suggest further behavioral assays.