Laura E. Mezey

The Spectral Main Sequence of Human Saccades

Despite the many models of saccadic eye movements, little attention has been paid to the shape of saccade trajectories. Some investigators have argued that saccades are driven by a rectangular “bang-bang” neural control signal, whereas others have emphasized the similarity to fast arm movement trajectories, such as the “minimum jerk” profile. However, models have not been tested rigorously against empirical trajectories. We examined the Fourier transforms of saccades and compared them with theoretical models. Horizontal saccades were recorded from 10 healthy subjects. The Fourier transform of each saccade was accurately computed using a padded fast Fourier transform (FFT), and the frequencies of the first three minima (M1, M2, M3) in each energy spectrum were measured to a precision of 0.12 Hz. Each subject showed near-linear trends in the relationships among M1, M2, and M3 and the reciprocal of duration (1/T), which we call the “spectral main sequence.” Extrapolation of plots did not pass through the origin, indicating a subtle departure from self-similarity. Bivariate confidence regions were established to allow for slope-intercept variability. The nonharmonic relationships seen cannot arise from a rectangular saccadic pulse driving a linear ocular plant. The relationships are also incompatible with minimum acceleration, minimum jerk, or higher-order minimum square derivative trajectories. The best fits were made by trajectories that minimize postmovement variance with signal-dependent noise (Harris and Wolpert, 1998). It is concluded that the spectral main sequence is exquisitely sensitive to the saccade trajectory and should be used to test objectively all present and future models of saccades.

The basis for using bone-conducted vibration or air-conducted sound to test otolithic function.

Extracellular single neuron recordings of primary vestibular neurons in Scarpas ganglion in guinea pigs show that low‐intensity 500 Hz bone‐conducted vibration (BCV) or 500 Hz air‐conducted sound (ACS) activate a high proportion of otolith irregular neurons from the utricular and saccular maculae but few semicircular canal neurons. In alert guinea pigs, and humans, 500 Hz BCV elicits otolith‐evoked eye movements. In humans, it also elicits a myogenic potential on tensed sternocleidomastoid muscles. Although BCV and ACS activate both utricular and saccular maculae, it is possible to probe the functional status of these two sense organs separately because of their differential neural projections. Saccular neurons have a strong projection to neck muscles and a weak projection to the oculomotor system. Utricular afferents have a strong projection to eye muscles. So measuring oculomotor responses to ACS and BCV predominantly probes utricular function, while measuring neck muscle responses to these stimuli predominantly probes saccular function.

Neural basis of new clinical vestibular tests: otolithic neural responses to sound and vibration.

Extracellular single neuron recording and labelling studies of primary vestibular afferents in Scarpas ganglion have shown that guinea‐pig otolithic afferents with irregular resting discharge are preferentially activated by 500 Hz bone‐conducted vibration (BCV) and many also by 500 Hz air‐conducted sound (ACS) at low threshold and high sensitivity. Very few afferent neurons from any semicircular canal are activated by these stimuli and then only at high intensity. Tracing the origin of the activated neurons shows that these sensitive otolithic afferents originate mainly from a specialized region, the striola, of both the utricular and saccular maculae. This same 500 Hz BCV elicits vestibular‐dependent eye movements in alert guinea‐pigs and in healthy humans. These stimuli evoke myogenic potentials, vestibular‐evoked myogenic potentials (VEMPs), which are used to test the function of the utricular and saccular maculae in human patients. Although utricular and saccular afferents can both be activated by BCV and ACS, the differential projection of utricular and saccular afferents to different muscle groups allows for differentiation of the function of these two sensory regions. The basic neural data support the conclusion that in human patients in response to brief 500 Hz BCV delivered to Fz (the midline of the forehead at the hairline), the cervical VEMP indicates predominantly saccular function and the ocular VEMP indicates predominantly utricular function. The neural, anatomical and behavioural evidence underpins clinical tests of otolith function in humans using sound and vibration.

Effect of Stimulus Rise-Time on the Ocular Vestibular-Evoked Myogenic Potential to Bone-Conducted Vibration

Objectives: The negative potential at 10 msec (called n10) of the ocular vestibular-evoked myogenic potential (oVEMP) recorded beneath the eyes in response to bone-conducted vibration (BCV) delivered to the skull at the midline in the hairline (Fz) is a new indicator of otolithic, and in particular utricular, function. Our aim is to find the optimum combination of frequency and rise-time for BCV stimulation, to improve the sensitivity of oVEMP testing in the clinic. Design: We tested 10 healthy subjects with 6 msec tone bursts of BCV at three stimulus frequencies, 250, 500, and 750 Hz, at rise-times ranging between 0 and 2 msec. The BCV was delivered at Fz. Results: The n10 response was significantly larger at the shorter rise-times, being largest at zero rise-time. In addition, we examined the effect of stimulus frequency in these same subjects by delivering 6 msec tone bursts at zero rise-time at a range of frequencies from 50 to 1200 Hz. The main effect of rise-time was significant with shorter rise-times leading to larger n10 responses and the Rise-Time × Frequency interaction was significant so that at low frequencies (100 Hz) shorter rise-times had a modest effect on n10 whereas at high frequencies (750 Hz) shorter rise-times increased n10 amplitude substantially. The main effect of frequency was also significant: The n10 response tended to be larger at lower frequency, being largest between 250 and 500 Hz. Conclusions: In summary, in this sample of healthy subjects, the most effective stimulus for eliciting oVEMP n10 to BCV at Fz was found to be a tone burst with a rise-time of 0 msec at low stimulus frequency (250 or 500 Hz).

Saccadic strategies in children with hemianopia

Multiple hypometric (undershooting) saccades are generally reported as a compensatory strategy in adults with homonymous hemianopia. However, hypermetric (overshooting) saccades have been reported to develop spontaneously as a beneficial strategy in response to predictable targets. We examined the saccades of 10 children (aged 5 to 16 years) with homonymous hemianopia to determine the type of compensatory eye‐movement strategies employed 6 months to 16 years after hemianopia onset. Homonymous hemianopia was identified using perimetry and/or pattern visual evoked potentials and supported with results of neuroimaging. Eye movements were recorded using bitemporal electrooculography. Saccades were elicited to a red light source in a semipredictable paradigm. We found that hypermetria was not a consistent compensatory strategy in our patients. In spite of the predictability of our paradigm and the long follow‐up period, multiple hypometric saccades into the blind field appeared to be the preferred strategy.

Adaptive Control of Saccades in Children with Dancing Eye Syndrome

Dancing eye syndrome (DES), or opsoclonus-myoclonus, is a rare neurological syndrome characterized by opsoclonus (spontaneous chaotic involuntary bursts of back-to-back saccades in all directions) and myoclonus (jerky involuntary movements of the limbs). Onset is usually in childhood, under 3 years of age. Although there can be good recovery from the acute symptoms, long-term neurological sequelae are often found.1,2 The etiology of DES is as yet unknown and may involve the brainstem and/or the cerebellum. A recent SPECT study of two children with DES has implicated the vermis of the cerebellum, in particular with the generation of opsoclonus.3 Shawkat et al. (1993) reported that visually guided reflexive saccades recorded from DES patients during the acute phase of their disease are hypermetric (gain >1).4 Saccadic dysmetria in humans is often associated with lesions of the vermis of the cerebellum and/or the deep cerebellar nuclei.5–7 Saccadic gain is under adaptive control (AC), which maintains the optimal accuracy of saccades with respect to their target, and it has been shown experimentally that the vermis of the cerebellum and fastigial nuclei in monkeys are necessary for AC.8 Given possible neuropathology in the cerebellum, and specifically the vermis, it is plausible that patients with DES may have chronic saccade dysmetria consistent with the failure of the saccadic AC system. We set out to test this hypothesis in a group of children and young adults with DES. A gain-decreasing intra-saccadic target perturbation paradigm was used to test the active functioning of the AC system.