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. 2013 Jul 3;33(27):11281-95.
doi: 10.1523/JNEUROSCI.3415-12.2013.

Keeping Your Head on Target

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Free PMC article

Keeping Your Head on Target

Aasef G Shaikh et al. J Neurosci. .
Free PMC article

Abstract

The mechanisms by which the human brain controls eye movements are reasonably well understood, but those for the head less so. Here, we show that the mechanisms for keeping the head aimed at a stationary target follow strategies similar to those for holding the eyes steady on stationary targets. Specifically, we applied the neural integrator hypothesis that originally was developed for holding the eyes still in eccentric gaze positions to describe how the head is held still when turned toward an eccentric target. We found that normal humans make head movements consistent with the neural integrator hypothesis, except that additional sensory feedback is needed, from proprioceptors in the neck, to keep the head on target. We also show that the complicated patterns of head movements in patients with cervical dystonia can be predicted by deficits in a neural integrator for head motor control. These results support ideas originally developed from animal studies that suggest fundamental similarities between oculomotor and cephalomotor control, as well as a conceptual framework for cervical dystonia that departs considerably from current clinical views.

Figures

Figure 1.
Figure 1.
Schematic for data analysis. A depicts typical raw head position data from a CD patient. The head position waveform had high amplitude jerky head oscillations and superimposed small sinusoidal oscillations. The first step was to interactively select a region of interest (green box in A). To analyze the large jerky oscillatory head movements, we identified drift of the head position in the region of interest between two red dots (B). The signal was then subject to a Savitzsky–Golay filter, and the time constant of drift in filtered head position was computed (C). To analyze the smaller sinusoidal oscillatory movements, the region of interest between two red dots (D) within the region of interest in the green box (A) was interactively selected and detrended (E). Time points of intersection of zero-line and the signal moving from negative to positive were determined. The difference of these time points was considered as period of oscillation, and the oscillation frequency was determined as the inverse of the time period. H, Initial head position; Hi, Initial head velocity; Tc, decay time constant; OHM, oscillatory head movements.
Figure 2.
Figure 2.
Holding the head on target under different conditions. For the condition with head-fixed laser plus LED target, subjects aligned the projection of laser fixed to the top of the head with a visible LED target (A–C). For the condition with LED target only, subjects turned the head and held it on target without the head-fixed laser (D–F). For the condition with vibration and LED target, gentle vibration was applied to the dorsal spinous processes of the neck to affect muscles on both sides (G–I). The last condition combined the head laser, neck vibration, and LED target (J–L). For actual head position traces, horizontal head positions are plotted along the ordinate and time along the abscissa (A, D, G, J). Head drift amplitudes are shown in B, E, H, and K. Initial head drift velocities are shown in C, F, I, and L. Drift amplitudes or velocities are plotted along y-axis, and eccentric head positions along x-axis. Each data point represents one drift movement, while each color depicts one subject. For all panels, positive values of head position indicate rightward head positions, and negative values indicate leftward head positions.
Figure 3.
Figure 3.
Decay time constants for head drifts according to degree of eccentricity. The amount of eccentricity did not affect the time constants.
Figure 4.
Figure 4.
A comparison of the two phases of head movement in normal subjects with a head fixed laser and neck vibration attempting to hold the head toward a specific LED target. A is a box-and-whisker plot summarizing the ratio of fast (quick-phase) and slow (drift) head movements. The horizontal line in the center of notch represents the median ratio, the whiskers represent the range, and symbols represent outliers. B shows the schematic of sinusoidal waveform for typical tremors, compared with the nonsinusoidal waveform for the jerky head movements. C illustrates the main-sequence analysis of corrective head movements (gray) of the quick phases compared with the main-sequence analysis for voluntary head saccades (black). The kinematics of quick phases and visually guided head saccades were compared by fitting each dataset to a power law function between amplitude and peak velocity. The data from both sources revealed no significant differences in this function, although those for the larger jerky head movements were smaller than those of the head saccades.
Figure 5.
Figure 5.
Rebound head nystagmus. A–D depict the head dynamics for a typical normal subject under each of the four test conditions. A depicts the condition with the head-fixed laser aimed at the LED light; the head was stable during both eccentric positions and after returning to the midline. B shows the condition with LED target but no laser. The addition of neck vibration is shown in C, while LED and head-fixed target plus neck vibration is shown in D. In B–D the rebound drifts were apparent when the head returned to the midline (B–D, highlighted yellow boxes). The drifts were not present in the condition including LED target plus laser, but were in the remaining three experimental paradigms. E–H objectively summarize all data from all subjects. The velocities for rebound head drifts are plotted on the y-axis with head position during prior eccentric head position along the x-axis. Each data point represents one rebound drift and each color depicts one subject. The negative values for head orientation depict leftward positions and the negative values for velocities represent leftward drifts. Rebound drifts were always directed opposite those evoked by holding eccentric positions, with positive slopes for all conditions. The data points and positive slope values indicate that leftward rebound drifts were associated with leftward head holding before return to midline, and vice versa.
Figure 6.
Figure 6.
An example of typical head movements in a patient with CD wearing a head-fixed laser and attempting to aim the head at specific LED targets. The head does not remain on target, but demonstrates a recurring cycle of slow drifts away from the target with rapid corrections back to target (A). Magnification of the gray box zone in A shows large amplitude OHM with a waveform that does not appear sinusoidal (B). Further magnification of the trace in B reveals a superimposed smaller OHM with a more sinusoidal waveform (C). Box-and-whisker plots show that these two different OHM have different amplitudes (D) and frequencies (E). In these plots, the central horizontal line represents the median, the height of the box represents the spread around the median, while the whiskers represent the range. The first type of OHM (B) has a larger amplitude and lower frequency than the second OHM (C). The median quick-phase/slow-phase (in case of sinusoidal oscillations faster to slower movement) ratio for the small OHM was close to 1.0 as expected for a sinusoidal waveform, while that for the larger OHM was significantly higher as expected for a nonsinusoidal waveform (F).
Figure 7.
Figure 7.
Head drift in a healthy subject and 14 patients with CD while aiming the head at LED targets with the aid of a head-fixed laser for accuracy. Torsional head positions (y-axis) were plotted against horizontal head position (x-axis). The circles show the initial target position and the lines depict drifts. Lines parallel to the abscissa represent pure horizontal drift and lines parallel to the ordinate pure torsional drift. The lines representing drifts often had an oblique component, indicating a combination of horizontal and torsional drifts. In healthy subjects head drifts were negligible, so the figure shows only circle symbols without lines (top). CD patients exhibited drift along all three axes (panels P1–P14). Gray dashed lines represent the horizontal coordinates of the mathematically derived null while red dashed lines are the horizontal coordinates of the clinical null.
Figure 8.
Figure 8.
Two different types of head drifts seen in patients with CD. These types are based on the direction of the head drift in relation to the null position. In both cases horizontal head position is plotted on the y-axis and time is plotted on the x-axis, and the bottom traces represent null position. The majority of patients had head drifts toward the null (A, B), while quick phases corrected for the drifts by bringing the head back to the desired orientation. In two patients, head drifts moved the head away from the null (C, D).
Figure 9.
Figure 9.
Relationship between drift velocity and null positions in CD. Blue data points depict horizontal drift velocity. Horizontal drift velocity in CD is minimal at the null position, and increases with distance from the null. There is a reversal in the drift direction as the head orientation shifts from the right of the null to the left. This phenomenon is reflected in the change in the sign of the drift velocity. Red and green data points depict relationships between torsional and vertical drift velocities with horizontal head position. Axes were customized for each patient to most clearly demonstrate the size and direction of drifts.
Figure 10.
Figure 10.
Relationship of horizontal decay time constant and eccentric head position during LED targeted paradigm (without visual feedback). The values of decay time constant are plotted along ordinate while horizontal head position is plotted on abscissa.
Figure 11.
Figure 11.
Characteristics of head drifts among CD patients attempting to aim the head at an LED target with or without a head-fixed laser. The amplitudes (A) and the frequencies (B) of cycles without the head-fixed laser are plotted on the y-axis while those with the head-fixed laser are plotted on the x-axis. Each data point represents one patient. Dashed line is an equality line. All data points depicting amplitude fell above the equality line, indicating significantly larger drift amplitudes without the laser (paired t test, p < 0.01). Data points representing frequency fell below the equality line, demonstrating a significantly lower frequency without the laser (paired t test; p < 0.05). The relationship between head amplitude and velocity of head movements is shown in C. Black symbols show the condition without the laser while open symbols show the condition with the laser. Visually guided head saccades from the same patients are shown in gray. The data from both sources overlapped suggesting similar kinematic properties.

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