Loss of balance during balance beam walking elicits a multifocal theta band electrocortical response

Abstract

Determining the neural correlates of loss of balance during walking could lead to improved clinical assessment and treatment for individuals predisposed to falls. We used high-density electroencephalography (EEG) combined with independent component analysis (ICA) to study loss of balance during human walking. We examined 26 healthy young subjects performing heel-to-toe walking on a treadmill-mounted balance beam as well as walking on the treadmill belt (both at 0.22 m/s). ICA identified clusters of electrocortical EEG sources located in or near anterior cingulate, anterior parietal, superior dorsolateral-prefrontal, and medial sensorimotor cortex that exhibited significantly larger mean spectral power in the theta band (4-7 Hz) during walking on the balance beam compared with treadmill walking. Left and right sensorimotor cortex clusters produced significantly less power in the beta band (12-30 Hz) during walking on the balance beam compared with treadmill walking. For each source cluster, we also computed a normalized mean time/frequency spectrogram time locked to the gait cycle during loss of balance (i.e., when subjects stepped off the balance beam). All clusters except the medial sensorimotor cluster exhibited a transient increase in theta band power during loss of balance. Cluster spectrograms demonstrated that the first electrocortical indication of impending loss of balance occurred in the left sensorimotor cortex at the transition from single support to double support prior to stepping off the beam. These findings provide new insight into the neural correlates of walking balance control and could aid future studies on elderly individuals and others with balance impairments.

Keywords: EEG; gait; independent component analysis; neural control; source analysis.

Fig. 1.

A sketch of the experimental setup showing a subject walking on a treadmill-mounted balance beam. A picture of the balance-beam treadmill is also shown (inset).

Fig. 2.

Clusters of independent component (IC) EEG sources localized in and near anterior cingulate (orange), posterior cingulate (2 clusters, magenta and cyan), superior dorsolateral-prefrontal (yellow), anterior parietal (green), left and right lateral sensorimotor (red), and medial sensorimotor (blue) cortex. Top: small spheres indicate the equivalent current dipole locations of each clustered IC source. Bottom: larger spheres show the locations of the cluster centroids.

Fig. 3.

A: grand average spectral power for each cluster of electrocortical sources during walking on the balance beam (red line) and walking on the treadmill belt (off the balance beam; blue line). The lowest frequency shown is 3 Hz. Significant differences in spectral power between the on-beam and off-beam conditions are indicated by the shaded regions: reddish (theta band) regions indicate larger power in balance beam walking; bluish regions (higher frequencies) indicate larger power in treadmill walking (P < 0.05). The colors of the plot titles correspond to the colors of the equivalent current dipoles in Fig. 2. DL-PFC, superior dorsolateral-prefrontal cortex. B: grand average normalized log spectrograms showing changes in spectral power during and after loss of balance relative to average spectral power during the last successful step prior to loss of balance (left of red vertical line). Mean step period (time between successive foot-to-ground contacts) was 1,100 ms. Four steps are shown; BC indicates foot-to-beam contact, and TC indicates foot-to-treadmill contact. After the second BC event, the subject loses balance and recovers by stepping off of the beam and onto the treadmill. Nonsignificant differences from baseline (P > 0.05) have been set to 0 dB (green). The colors of the plot titles correspond to the colors of the equivalent current dipoles and dipole clusters in Fig. 2. The left sensorimotor cluster plot averages only those trials in which a loss of balance occurred toward the right side of the beam; the right sensorimotor cluster plot averages only those trials in which a loss of balance occurred toward the left side of the beam. All other results shown here average all trials when a loss of balance occurred, both to the left and to the right. Theta spectral power increases began in the left sensorimotor sources, followed by the posterior cingulate, anterior cingulate, and right sensorimotor sources, and finally in anterior parietal and superior dorsolateral-prefrontal sources.

Fig. 4.

Timing comparison of mean sensorimotor source cluster changes in EEG spectral power, lower leg electromyography (EMG), and center of mass motion for losses of balance to the left side of the beam. Four steps are shown. After the second BC (black vertical line), the subject loses balance and recovers by stepping off of the beam and onto the treadmill. For the sensorimotor cluster EEG spectral changes, nonsignificant differences from baseline (P > 0.05) have been set to 0 dB (green); the lowest frequency shown is 3 Hz. For the lower limb EMG and center of mass position data, red lines show loss-of-balance trial averages, blue lines are on-beam walking averages, and dashed lines indicate +1 standard deviation. The cluster dipole images are replicated from Fig. 3.

Fig. 5.

Timing comparison of mean sensorimotor source cluster changes in EEG spectral power, lower leg EMG, and center of mass motion for losses of balance to the right side of the beam. Four steps are shown. After the second BC (black vertical line), the subject loses balance and recovers by stepping off of the beam and onto the treadmill. For the sensorimotor cluster EEG spectral changes, nonsignificant differences from baseline (P > 0.05) have been set to 0 dB (green); the lowest frequency shown is 3 Hz. For the lower limb EMG and center of mass position data, red lines show loss-of-balance trial averages, blue lines are on-beam walking averages, and dashed lines indicate +1 standard deviation. The cluster dipole images are replicated from Fig. 3.

Fig. 6.

Grand average normalized log spectrograms during walking off and on the balance beam (Treadmill and Balance Beam, respectively). Two steps are shown, with RTC indicating right foot-to-treadmill contact and LTC indicating left foot-to-treadmill contact. Mean step period was 1,100 ms. Nonsignificant differences from baseline (P > 0.05) have been set to 0 dB (green). The colors of the plot titles correspond to the colors of the equivalent current dipoles and dipole clusters in Fig. 2. There were no substantial changes in theta spectral power during treadmill walking or balance beam walking compared with those seen during loss of balance on the balance beam (Figs. 3–5).