A new approach to quantifying the EEG during walking: Initial evidence of gait related potentials and their changes with aging and dual tasking.

BACKGROUND: The electroencephalogram (EEG) can be a useful tool to investigate the neurophysiology of gait during walking. Our aims were to develop an approach that identify and quantify event related potentials (ERPs) during a gait cycle and to examine the effects of aging and dual tasking on these gait related potentials (GRPs). METHODS: 10 young and 10 older adults walked on a treadmill while wearing a wireless 20-channels EEG and accelerometers on the ankles. Each heel strike extracted from the accelerometers was used as an event to which the electrical brain activity pattern was locked. The subjects performed usual and dual task walking that included an auditory oddball task. GRPs amplitude and latency were computed, and a new measure referred to as Amplitude Pattern Consistency (APC) was developed to quantify the consistency of these GRP amplitudes within a gait cycle. The results were compared between and within groups using linear mixed model analysis. RESULTS: The electrical pattern during a gait cycle consisted of two main positive GRPs. Differences in these GRPs between young and older adults were observed in Pz and Cz. In Pz, older adults had higher GRPs amplitude (p = 0.006, p = 0.010), and in Cz lower APC (p = 0.025). Alterations were also observed between the walking tasks. Both groups showed shorter latency during oddball walking compared to usual walking in Cz (p = 0.040). In addition, the APC in Cz was correlated with gait speed (r = 0.599, p = 0.011) in all subjects and with stride time variability in the older adults (r = -0.703, p = 0.023). CONCLUSIONS: This study is the first to define specific gait related potentials within a gait cycle using novel methods for quantifying waveforms. Our findings show the potential of this approach to be applied broadly to study the EEG during gait in a variety of contexts. The observed changes in GRPs with aging and walking task and the relationship between GRPs and gait may suggest the neurophysiologic foundation for studying walking and for developing new approaches for improving gait.

3D hand motion trajectory prediction from EEG mu and beta bandpower.

A motion trajectory prediction (MTP) - based brain-computer interface (BCI) aims to reconstruct the three-dimensional (3D) trajectory of upper limb movement using electroencephalography (EEG). The most common MTP BCI employs a time series of bandpass-filtered EEG potentials (referred to here as the potential time-series, PTS, model) for reconstructing the trajectory of a 3D limb movement using multiple linear regression. These studies report the best accuracy when a 0.5-2Hz bandpass filter is applied to the EEG. In the present study, we show that spatiotemporal power distribution of theta (4-8Hz), mu (8-12Hz), and beta (12-28Hz) bands are more robust for movement trajectory decoding when the standard PTS approach is replaced with time-varying bandpower values of a specified EEG band, ie, with a bandpower time-series (BTS) model. A comprehensive analysis comprising of three subjects performing pointing movements with the dominant right arm toward six targets is presented. Our results show that the BTS model produces significantly higher MTP accuracy (R~0.45) compared to the standard PTS model (R~0.2). In the case of the BTS model, the highest accuracy was achieved across the three subjects typically in the mu (8-12Hz) and low-beta (12-18Hz) bands. Additionally, we highlight a limitation of the commonly used PTS model and illustrate how this model may be suboptimal for decoding motion trajectory relevant information. Although our results, showing that the mu and beta bands are prominent for MTP, are not in line with other MTP studies, they are consistent with the extensive literature on classical multiclass sensorimotor rhythm-based BCI studies (classification of limbs as opposed to motion trajectory prediction), which report the best accuracy of imagined limb movement classification using power values of mu and beta frequency bands. The methods proposed here provide a positive step toward noninvasive decoding of imagined 3D hand movements for movement-free BCIs.

E3D hand movement velocity reconstruction using power spectral density of EEG signals and neural network.

Three dimensional (3D) limb motion trajectory is predictable with a non-invasive brain-computer interface (BCI). To date, most non-invasive motion trajectory prediction BCIs use potential values of electroencephalographic (EEG) signals as the input to a multiple linear regression (mLR) based kinetic data estimator. We investigated the possible improvement in accuracy of 3D hand movement prediction (i.e., the correlation of registered and reconstructed hand velocities) by replacing raw EEG potentials with spectrum power values of specific EEG bands. We also investigated if a non-linear neural network based estimator outperformed the mLR approach. The spectrum power model provided significantly higher accuracy (R~0.60) compared to the similar EEG potentials based approach (R~0.45). Additionally, when replacing the mLR based kinetic data estimation module with a feed-forward neural network (NN) we found the NN based spectrum power model provided higher accuracy (R~0.70) compared to the similar mLR based approach (R~0.60).

Temporal frequency of whisker movement. I. Representations in brain stem and thalamus.

How does processing of information change the internal representations used in subsequent stages of sensory pathways? To approach this question, we studied the representations of whisker movements in the lemniscal and paralemniscal pathways of the rat vibrissal system. We recently suggested that these two pathways encode movement frequency in different ways. We proposed that paralemniscal thalamocortical circuits, functioning as phase-locked loops (PLLs), translate temporally coded information into a rate code. Here we focus on the two major trigeminal nuclei of the brain stem, nucleus principalis and subnucleus interpolaris, and on their thalamic targets, the ventral posteromedial nucleus (VPM) and the medial division of the posterior nucleus (POm). This is the first study in which these brain stem and thalamic nuclei were explored together in the same animals and using the same stimuli. We studied both single- and multi-unit activity. We moved the whiskers both mechanically and by air puffs; here we present air-puff-induced movements because they are more similar to natural movements than movements induced by mechanical stimulations. We describe the basic properties of the responses in these brain stem and thalamic nuclei. The responses in both brain stem nuclei were similar; responses to air puffs were mostly tonic and followed the trajectory of whisker movement. The responses in the two thalamic nuclei were similar during low-frequency stimulations or during the first pulses of high-frequency stimulations, exhibiting more phasic responses than those of brain stem neurons. However, with frequencies >2 Hz, VPM and POm responses differed, generating different representations of the stimulus frequency. In the VPM, response amplitudes (instantaneous firing rates) and spike counts (total number of spikes per stimulus cycle) decreased as a function of the frequency. In the POm, latencies increased and spike count decreased as a function of the frequency. Having described the basic response properties in the four nuclei, we then focus on a specific test of our PLL hypothesis for coding in the paralemniscal pathway. We used short-duration air puffs, much shorter than whisker movements during natural whisking. The activity in this situation was consistent with the prediction we made on the basis of the PLL hypothesis.

Temporal frequency of whisker movement. II. Laminar organization of cortical representations.

Part of the information obtained by rodent whiskers is carried by the frequency of their movement. In the thalamus of anesthetized rats, the whisker frequency is represented by two different coding schemes: by amplitude and spike count (i.e., response amplitudes and spike counts decrease as a function of frequency) in the lemniscal thalamus and by latency and spike count (latencies increase and spike counts decrease as a function of frequency) in the paralemniscal thalamus (see accompanying paper). Here we investigated neuronal representations of the whisker frequency in the primary somatosensory ("barrel") cortex of the anesthetized rat, which receives its input from both the lemniscal and paralemniscal thalamic nuclei. Single and multi-units were recorded from layers 2/3, 4 (barrels only), 5a, and 5b during vibrissal stimulation. Typically, the input frequency was represented by amplitude and spike count in the barrels of layer 4 and in layer 5b (the "lemniscal layers") and by latency and spike count in layer 5a (the "paralemniscal layer"). Neurons of layer 2/3 displayed a mixture of the two coding schemes. When the pulse width of the stimulus was reduced from 50 to 20 ms, the latency coding in layers 5a and 2/3 was dramatically reduced, while the spike-count coding was not affected; in contrast, in layers 4 and 5b, the latencies remained constant, but the spike counts were reduced with 20-ms stimuli. The same effects were found in the paralemniscal and lemniscal thalamic nuclei, respectively (see accompanying paper). These results are consistent with the idea that thalamocortical loops of different pathways, although terminating within the same cortical columns, perform different computations in parallel. Furthermore, the mixture of coding schemes in layer 2/3 might reflect an integration of lemniscal and paralemniscal outputs.

Acetylcholine-dependent induction and expression of functional plasticity in the barrel cortex of the adult rat.

The involvement of acetylcholine (ACh) in the induction of neuronal sensory plasticity is well documented. Recently we demonstrated in the somatosensory cortex of the anesthetized rat that ACh is also involved in the expression of neuronal plasticity. Pairing stimulation of the principal whisker at a fixed temporal frequency with ACh iontophoresis induced potentiations of response that required re-application of ACh to be expressed. Here we fully characterize this phenomenon and extend it to stimulation of adjacent whiskers. We show that these ACh-dependent potentiations are cumulative and reversible. When several sensori-cholinergic pairings were applied consecutively with stimulation of the principal whisker, the response at the paired frequency was further increased, demonstrating a cumulative process that could reach saturation levels. The potentiations were specific to the stimulus frequency: if the successive pairings were done at different frequencies, then the potentiation caused by the first pairing was depotentiated, whereas the response to the newly paired frequency was potentiated. During testing, the potentiation of response did not develop immediately on the presentation of the paired frequency during application of ACh: the analysis of the kinetics of the effect indicates that this process requires the sequential presentation of several trains of stimulation at the paired frequency to be expressed. We present evidence that a plasticity with similar characteristics can be induced for responses to stimulation of an adjacent whisker, suggesting that this potentiation could participate in receptive field spatial reorganizations. The spatial and temporal properties of the ACh-dependent plasticity presented here impose specific constraints on the underlying cellular and molecular mechanisms.

Transformation from temporal to rate coding in a somatosensory thalamocortical pathway.

The anatomical connections from the whiskers to the rodent somatosensory (barrel) cortex form two parallel (lemniscal and paralemniscal) pathways. It is unclear whether the paralemniscal pathway is directly involved in tactile processing, because paralemniscal neuronal responses show poor spatial resolution, labile latencies and strong dependence on cortical feedback. Here we show that the paralemniscal system can transform temporally encoded vibrissal information into a rate code. We recorded the representations of the frequency of whisker movement along the two pathways in anaesthetized rats. In response to varying stimulus frequencies, the lemniscal neurons exhibited amplitude modulations and constant latencies. In contrast, paralemniscal neurons in both thalamus and cortex coded the input frequency as changes in latency. Because the onset latencies increased and the offset latencies remained constant, the latency increments were translated into a rate code: increasing onset latencies led to lower spike counts. A thalamocortical loop that includes cortical oscillations and thalamic gating can account for these results. Thus, variable latencies and effective cortical feedback in the paralemniscal system can serve the processing of temporal sensory cues, such as those that encode object location during whisking. In contrast, fixed time locking in the lemniscal system is crucial for reliable spatial processing.

A neuronal analogue of state-dependent learning.

State-dependent learning is a phenomenon in which the retrieval of newly acquired information is possible only if the subject is in the same sensory context and physiological state as during the encoding phase. In spite of extensive behavioural and pharmacological characterization, no cellular counterpart of this phenomenon has been reported. Here we describe a neuronal analogue of state-dependent learning in which cortical neurons show an acetylcholine-dependent expression of an acetylcholine-induced functional plasticity. This was demonstrated on neurons of rat somatosensory 'barrel' cortex, whose tunings to the temporal frequency of whisker deflections were modified by cellular conditioning. Pairing whisker stimulation with acetylcholine applied iontophoretically yielded selective lasting modification of responses, the expression of which depended on the presence of exogenous acetylcholine. Administration of acetylcholine during testing revealed frequency-specific changes in response that were not expressed when tested without acetylcholine or when the muscarinic antagonist, atropine, was applied concomitantly. Our results suggest that both acquisition and recall can be controlled by the cortical release of acetylcholine.

Simultaneous multi-site recordings and iontophoretic drug and dye applications along the trigeminal system of anesthetized rats.

A multi-electrode system that permits simultaneous recordings from multiple neurons and iontophoretic applications at two or three different brain sites during acute experiments is described. This system consists of two or three microdrive terminals, each of which includes four electrodes that can be moved independently and used for both extracellular recordings and microiontophoretic drug administration. Drug applications were performed during standard extracellular recordings of multiple single-units via specialized combined electrodes (CEs), which enable ejection of neuroactive substances and recording of neuronal activity from the same electrode. With this system, we were able to successfully record simultaneously from different levels (brainstem, thalamus, and cortex) of the vibrissal ascending pathway of the anesthetized rat. Herein, examples of simultaneous recordings from the brainstem and thalamus and from the thalamus and cortex are presented. An effect of iontophoretic applications of agonists and antagonists of metabotropic glutamate receptors (mGluRs) in the thalamus is demonstrated, and the extent of drug diffusion in the barrel cortex is demonstrated with biocytin. This new multi-electrode system will facilitate the study of transformations of sensory information acquired by the whiskers into cortical representations.