Abstract

Under normal circumstances, tracking of small moving visual objects is done by eye and head movements. Head movements induce the vestibulo-ocular reflex (VOR), which drives the eyes in the direction opposite to the eye movements. During visual tracking the VOR has to be suppressed, and it is assumed that the central nervous system actually generates a smooth pursuit signal to cancel the VOR [9]. Thus, a SPEM deficit is generally accompanied by impaired VOR suppression.

Usually SPEM are tested with sinusoidal stimuli which only refer to steady state conditions. They are different from the initial 20–40 ms, when SPEM are independent from stimulus parameters. To account for the different motor programs on a neuronal level for SPEM generation, often the step-ramp (Rashbass) paradigm is used. So far, only few clinical studies addressed the question of partial dysfunction in SPEM generation [10].

Both SPEM and saccades are voluntary eye movements. Traditionally they have been considered as two distinct systems. However, it is becoming increasingly evident that both types of eye movements share similar anatomical networks at the cortical and subcortical level. These networks are presumably used for selection processes involving attention, perception, memory and expectation [11].

Optokinetic Response

Large moving visual fields (with the head stationary) lead to slow compensatory eye movements. These eye movements are driven by the optokinetic system. During continuous motion of the visual surround, fast resetting eye movements occur, which are basically saccades. The combination of slow compensatory and fast resetting eye movements is called optokinetic nystagmus (OKN), the direction being labeled after the fast phase.

Two components can be distinguished in the generation of the slow compensatory phase [12]. One is called the ‘direct’ component, because it occurs directly after the onset of the optokinetic stimulus and is considered to reflect the ocular following response (OFR) [13]. It can best be demonstrated by the rapid increase in slow-phase eye velocity after the sudden presentation of a constant optokinetic stimulus. In contrast, the second component is called the ‘indirect’ component, because it leads to a more gradual increase in slow-phase eye velocity during continuous stimulation. The best demonstration of the ‘indirect’ component alone is optokinetic after-nystagmus (OKAN) – the nystagmus that continues in the dark after the light has been turned off [12]. The ‘indirect’ or ‘velocity storage’ component can be related to concomitant activity changes in the vestibular nuclei [14–16].

There is also some evidence that the ‘direct’ component is more involved in translational optical flow in contrast to rotational optical flow for the ‘indirect’ component [17].

In birds and lateral-eyed animals (rat, rabbit) the optokinetic response consists almost entirely of the ‘indirect’ component. In the monkey, both components are well developed, and maximal OKN velocities can reach more than 180 /s [12, 18]. In contrast, in humans the ‘indirect’ component is often weak (as indicated by OKAN), variable, and sometimes virtually missing [3, 19].

Maximal OKN velocities in the horizontal plane seldom exceed 120 /s in humans and can be mainly related to the ‘direct’ component. Clinically, values above 60 /s are considered normal [3]. There seems to be some age-related decline in OKN responses for subjects aged 75 years [8]. At constant stimulus velocities below 60 /s, the gain (eye/stimulus velocity) is about 0.8 [20]. Responses can still be obtained at sinusoidal stimulation above 1 Hz [21]. OKN is also used to determine residual visual capacities in patients with severe motor and intellectual disabilities [22].

Vertical OKN has been less intensively investigated. In general, vertical OKN is slower than horizontal OKN and upward stimulation is more effective than downward stimulation [23]. At the bedside, normal function can be assumed as long as up and down OKN can be elicited. In the upright body position, vertical OKAN is often missing or only present after upward optokinetic stimulation [23]. With a rotating visual field, also torsional OKN with a low gain ( 0.2) can be elicited [24, 25].

Ocular Following Response

The immediate involuntary response to a large moving visual field is called OFR. OFR in humans can have latencies as short as 60–70 ms, which are shorter than those for SPEM. The size of the visual stimulus and the involuntary character are further features to distinguish these eye movements. The OFR is functionally linked to the translational VOR in contrast to OKN being related to the rotational VOR [26]. Experiments in humans with moving square waves and stimuli, in which the fundamental frequency of the square wave pattern was removed, revealed that the eyes always move in the direction of the strongest Fourier component, which is in the latter case the third harmonic. Under these conditions the eyes can move in the opposite direction (due to the third harmonic) of the movement of the general stimulus pattern [27]. Longer interstimulus intervals can reverse the direction of the OFR [27]. These findings support the hypothesis that visual motion detection for OFR is sensed by low-level (energy-based) rather than feature-based (high-level) mechanisms [28]. The middle temporal visual area (MT) and medial superior temporal visual area (MST) appear to be early cortical stages involved in motion responses [29] and in the initiation of OFR [30].