Overall, our results demonstrate proficient, continuous BMI control using LFPs and provide insight into the subject-specific spectral patterns of LFP activity modulated during control.
Neurons in the brain form highly complex networks through synaptic connections. Traditionally, functional connectivity between neurons has been explored using methods such as correlations, which do not contain any notion of directionality. Recently, an information-theoretic approach based on directed information theory has been proposed as a way to infer the direction of influence. However, it is still unclear whether this new approach provides any additional insight beyond conventional correlation analyses. In this paper, we present a modified procedure for estimating directed information and provide a comparison of results obtained using correlation analyses on both simulated and experimental data. Using physiologically realistic simulations, we demonstrate that directed information can outperform correlation in determining connections between neural spike trains while also providing directionality of the relationship, which cannot be assessed using correlation. Secondly, applying our method to rodent and primate data sets, we demonstrate that directed information can accurately estimate the conduction delay in connections between different brain structures. Moreover, directed information reveals connectivity structures that are not captured by correlations. Hence, directed information provides accurate and novel insights into the functional connectivity of neural ensembles that are applicable to data from neurophysiological studies in awake behaving animals.
Closed-loop decoder adaptation (CLDA) is an emerging paradigm for both improving and maintaining online performance in brain-machine interfaces (BMIs). The time required for initial decoder training and any subsequent decoder recalibrations could be potentially reduced by performing continuous adaptation, in which decoder parameters are updated at every time step during these procedures, rather than waiting to update the decoder at periodic intervals in a more batch-based process. Here, we present recursive maximum likelihood (RML), a CLDA algorithm that performs continuous adaptation of a Kalman filter decoder's parameters. We demonstrate that RML possesses a variety of useful properties and practical algorithmic advantages. First, we show how RML leverages the accuracy of updates based on a batch of data while still adapting parameters on every time step. Second, we illustrate how the RML algorithm is parameterized by a single, intuitive half-life parameter that can be used to adjust the rate of adaptation in real time. Third, we show how even when the number of neural features is very large, RML's memory-efficient recursive update rules can be reformulated to also be computationally fast so that continuous adaptation is still feasible. To test the algorithm in closed-loop experiments, we trained three macaque monkeys to perform a center-out reaching task by using either spiking activity or local field potentials to control a 2D computer cursor. RML achieved higher levels of performance more rapidly in comparison to a previous CLDA algorithm that adapts parameters on a more intermediate timescale. Overall, our results indicate that RML is an effective CLDA algorithm for achieving rapid performance acquisition using continuous adaptation.
Redundant encoding of information facilitates reliable distributed information processing. To explore this hypothesis in the motor system, we applied concepts from information theory to quantify the redundancy of movement-related information encoded in the macaque primary motor cortex (M1) during natural and neuroprosthetic control. Two macaque monkeys were trained to perform a delay center-out reaching task controlling a computer cursor under natural arm movement (manual control, 'MC'), and using a brain-machine interface (BMI) via volitional control of neural ensemble activity (brain control, 'BC'). During MC, we found neurons in contralateral M1 to contain higher and more redundant information about target direction than ipsilateral M1 neurons, consistent with the laterality of movement control. During BC, we found that the M1 neurons directly incorporated into the BMI ('direct' neurons) contained the highest and most redundant target information compared to neurons that were not incorporated into the BMI ('indirect' neurons). This effect was even more significant when comparing to M1 neurons of the opposite hemisphere. Interestingly, when we retrained the BMI to use ipsilateral M1 activity, we found that these neurons were more redundant and contained higher information than contralateral M1 neurons, even though ensembles from this hemisphere were previously less redundant during natural arm movement. These results indicate that ensembles most associated to movement contain highest redundancy and information encoding, which suggests a role for redundancy in proficient natural and prosthetic motor control.
It is plausible to hypothesize that the spiking responses of certain neurons represent functions of the spiking signals of other neurons. A natural ensuing question concerns how to use experimental data to infer what kind of a function is being computed. Model-based approaches typically require assumptions on how information is represented. By contrast, information measures are sensitive only to relative behavior: information is unchanged by applying arbitrary invertible transformations to the involved random variables. This paper develops an approach based on the information bottleneck method that attempts to find such functional relationships in a neuron population. Specifically, the information bottleneck method is used to provide appropriate compact representations which can then be parsed to infer functional relationships. In the present paper, the parsing step is specialized to the case of remapped-linear functions. The approach is validated on artificial data and then applied to recordings from the motor cortex of a macaque monkey performing an arm-reaching task. Functional relationships are identified and shown to exhibit some degree of persistence across multiple trials of the same experiment.
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