Exp Brain Res (1991) 83:471-476
Experimental BrainResearch 9
Springer-Verlag1991
Pursuit afternystagmus asymmetry in humans Avi Chaudhuri The Salk Institute for Biological Studies, San Diego, CA 92138-9216, USA Received March 5, 1990 / Accepted August 20, 1990
Summary. It is known that prolonged unidirectional motion of a large field induces a reflexive drift of the eyes in the same direction when the stimulus is turned off. The phenomenon, which is called optokinetic afternystagmus, is known to be stronger after upward than downward stimulus motion. It is now reported that a similar anisotropy exists in the afternystagmus associated with the smooth pursuit system (PAN). The speed of the PAN reflexive drift was found to be greater following upward tracking at all times tested during a 15 s interval when compared to the values following downward tracking. A psychophysical measure of illusory motion, presumed to be generated by suppression of PAN in order to maintain fixation upon a stationary target, also showed a significantly greater amplitude and duration for the upward direction. If the directional asymmetry is a property of a velocity integrator that is believed to generate the afternystagmus, then the results are compatible with the existence of a common integrator for both optokinetic and pursuit systems. Key words: Optokinetic - OKN - Integrator - Motion Aftereffect Human
Introduction In humans and non-human primates, there appear to be two components of optokinetic nystagmus (OKN) (Cohen et al. 1977; Raphan et al. 1979; Lisberger et al. 1981). At the onset of stimulus motion, an abrupt change in eye velocity takes place that just falls short of matching the stimulus velocity. This is followed by a more gradual increase in slow-phase velocity that ultimately results in steady-state OKN. The two components have been called the "direct" and "indirect" mechanisms respectively, terminology that is derived from models of the OKN process (Cohen et al. 1977). From the results of lesion 9 studies, it is thought that neural mechanisms subserving the "direct" component of OKN also mediate smooth
pursuit (Zee et al. 1976; Waespe et al. 1983; May et al. 1988), a mechanism that enables primates to track small objects that are moving with respect to the retina. It has been suggested that a cortico-ponto-cerebellar pathway has evolved in foveate animals that subserves the "direct" mechanism and which is superimposed upon a phylogenetically older brainstem mechanism that subserves the "indirect" pathway (Cohen et al. 1981; May et al. 1988). In animals that lack a fovea, slow-phase OKN velocity develops gradually and is believed to be produced primarily by the activation of the "indirect" pathway (Collewijn 1972; Evinger and Fuchs 1978; Hess et al. 1985). Two interesting properties of OKN have been described. When the inducing stimulus is eliminated after a period of OKN, the eyes continue to drift in the same direction, the duration being determined by the preceding OKN duration and velocity. This phenomenon and the ensuing gradual decline in slow-phase velocity is seen only in total darkness and has been termed optokinetic afternystagmus (OKAN). It is believed that a velocity storage integrator in the "indirect" pathway acts as a capacitor and begins to accumulate charge at the onset of O K N (Cohen et al. 1977; Cohen et al. 1990). According to this model, OKAN is the consequence of the discharge of this integrator. Lesion studies and singleunit recordings have tentatively identified the vestibular nuclei and the nucleus prepositus hypoglossi as the neural sites of the integrator (Waespe and Henn 1977; Cheron et al. 1986, Cannon and Robinson 1987). Both of these structures are known to have extensive interconnections with other components of the oculomotor system (Brodal 1984; McCrea et al. 1987; Belknap and McCrea 1988). Another feature of OKN is a directional asymmetry along the vertical axis. It has been shown in a number of species that upward pattern movement generates a higher gain O K N than downward movement (Collins et al. 1970; Matsuo and Cohen 1984; Wallman and Velez 1985). This has also been recently demonstrated in humans (Van den Berg and Collewijn 1988; Murasugi and
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Howard 1989). The OKN asymmetry is believed to be a property of the "indirect" pathway because a similar asymmetry is found in OKAN in humans and monkeys (Matsuo et al. 1979; Baloh et al. 1983; Murasugi and Howard 1989). Prolonged upward OKN (slow-phase direction) generates a strong afternystagmus whereas it is very weak or absent following downward movement. It is not clear if the asymmetry is a property of the velocity storage integrator or the neural elements that directly or indirectly feed into it. It has been shown, however, that the large majority of cells in the lateral terminal nucleus, an important relay station for vertical OKN (Simpson et al. 1979), are tuned for upward stimulus motion (Mustari et al. 1988; Mustari and Fuchs
1989). The notion that velocity storage, and its associated afternystagmus, is only a property of the "indirect" pathway has required some re-evaluation after the demonstration of a similar afternystagmus following a prolonged period of undirectional smooth pursuit. There are two components to the residual drift which ensues after the stimulus is extinguished. Initially, there is an abrupt drop in eye velocity (Mitrani and Dimitrov 1978; Bahill and McDonald 1983), the temporal characteristics of which appear to be related to the inertial properties of the eyeball when the pursuit drive is removed (Robinson 1965; Jell et al. 1987). This transient drift is accompanied by an afternystagmus with a much larger time constant and is in the same direction (Muratore and Zee 1979; Lisberger et al. 1981). This component is similar to OKAN and appears to be driven by the discharge of a velocity integrator (Muratore and Zee 1979). It is not presently known if the smooth pursuit system ("direct" pathway) has a velocity integrator of its own or whether it shares one with the "indirect" pathway. We now report the presence of an asymmetry in vertical pursuit afternystagmus (PAN) that is similar to OKAN asymmetry. The nature of this afternystagmus and its asymmetry will be documented by way of eye movement records following prolonged pursuit as well as by a psychophysical measure. The implications of this result with regard to the neural mechanisms of smooth pursuit and OKN will be discussed.
Methods The displays used in this study are illustrated in Fig. 1. In order to produce pursuit afternystagmus, subjects tracked a small target in a particular direction upon a totally dark background. The target velocity was 7.5 deg/s and the total excursion of the ramp was 7.5 deg. After one minute of tracking, either the tracking target was eliminated, leaving a totally dark field, or it was stopped and centered. The first test condition is necessary in order to see the eye drifts associated with pursuit afternystagmus. The second condition allows a psychophysical assessment of PAN, as described later. The stimuli for these experiments were generated on a PC installed with a graphics co-processor (Number Nine Computer Corp., Cambridge, MA) and displayed on a Zenith flat-screen color monitor. A total of eight subjects participated in various aspects of this study. Formal testing, including eye movement monitoring, was carried out on three of these observers. In order to ensure that motion of environmental contours did not interfere with the study,
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B Fig. 1A, B. Stimulus conditions used in showing PAN asymmetry along the vertical axis. Following either upward or downward pursuit for one minute, the tracking target vanished leaving only a dark field (Test 1). In the second condition, the target was stopped and centered after a similar period of pursuit (Test 2). Eight subjects were asked to fixate this target and report the nature of any illusory motion. Eye movements were collected during both adaptation and test periods in three subjects. In the same three subjects, the strength of the PAN generated illusory motion was determined by estimating its total duration and velocity at selected intervals
great care was taken to produce a totally dark visual field. The only stimulus present was the tracking target. This was accomplished by having the subjects look at the monitor through a tunnel (length 57 cm; diameter - 16 cm) that was placed against the screen. This eliminated all contours, even in the far periphery. A sheet of red acetate was placed on the monitor screen to remove any residual background radiation. The tracking/fixation target was a red square (8 rain arc). All subjects viewed the display binocularly in a dark room and in the upright position using a chin-rest and forehead support. Eye movement monitoring was done with the magnetic searchcoil technique (Robinson 1963; Collewijn et al. 1975) on three subjects. The observer was placed within a magnetic field which induced current upon eye movements in a search coil that was implanted within a contact lens (Skalar, Holland). Synchronous demodulation of axis-specific frequency signals provided accurate estimates of both horizontal and vertical eye movements (CNC Engineering, Seattle, WA). The coil itself was wound within a soft annular shaped contact lens that was placed in the right eye, which was anaesthetized with Proparacaine HC1 (0.5%). The duration of a typical experiment was 30 rain during which 5 trials were randomly presented for each of three directions of pursuit. The oculographic traces were analyzed off-line at the end of the experiment in order to obtain eye drift velocity. The subjects did not have any history of oculomotor dysfunction. Furthermore, no cases of spontaneous nystagmus were observed prior to tracking. A psychophysical assessment of vertical asymmetry was performed by measuring the duration and temporal profile of an illusory motion believed to be associated with PAN. The exponential decay of the illusory motion of the stationary tracking target was estimated following one minute of upward and downward pursuit by a nulling technique in which subjects were required to offtset the illusory motion by continually adjusting the speed of the target in the opposite direction so that it appeared stationary. In other words, the target had to be physically moved in the opposite direction in order to counteract the illusory motion and give the impression that it was stationary. The speed of the target was taken to be the same as that of the illusory motion and sampled at 500 ms intervals by the computer that generated the display. The same three subjects who participated in the search-coil experiments performed this task. A total of 5 trials were randomly presented for both upward and downward pursuit. The duration of the illusory drift was measured in 3 subjects. At the end of the tracking period, the target was stopped and centered. The subjects were now required to indicate by way of a key press, the cessation of any illusory motion. A computer driven stopwatch provided the duration, Subjects were instructed to use the same criterion, to the best of their ability, in judging the end of
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shown in Fig. 3a. The x-axis in this plot represents the time from the onset of afternystagmus (arrows in Fig. 2). These speed profiles were obtained by differentiating the eye movement traces of Fig. 2 with respect to time in 100 ms bins at selected intervals during the PAN period. The slow-phase speed of PAN following upward tracking was found to be significantly greater (p<0.05; t-test,
the illusory motion from one display to another. All trials were randomly interleaved with those that were part of another related study involving illusory motion (Chaudhuri. 1990).
Results The eye movement record of a typical response for three directions of tracking is shown in Fig. 2. All three subjects showed similar results in all trials and therefore only a representative record will be shown. As can be seen from the traces, near perfect smooth pursuit is generated during the adaptation period with the stimulus conditions that were used. The portion of the records to the left of the arrows, which represents the last few seconds of a one minute period of tracking, shows a smooth ramp with no large amplitude correcting saccades (gain = 1.0). At the point in the records indicated by the arrows, the tracking target was eliminated and observers were left staring into a completely dark field. The afternystagmus that was produced during this period was always in the direction of the prior pursuit. The PAN magnitude was seen to be greatest following upward pursuit in all three subjects than for downward pursuit. There was no evidence of this direction becoming reversed, a phenomenon that is often seen with O K A N (Aschan et al. 1956; Himi et al. 1988). However, as with OKAN, a dark field was required in order to evoke the afternystagmus. The presence of any visible contours or a lighted background attenuated the afternystagmus significantly, a phenomenon that has been termed "dumping" with regard to the OKAN process (Cohen et al. 1977). The temporal characteristics of pursuit afternystagmus decay in the upward and downward direction are
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n = 5) than downward tracking at all of the measured points within the first 15 seconds as the afternystagmus exponentially decayed to zero. All three subjects that were tested showed a similar asymmetry. Furthermore, the velocity at the onset of PAN was about 2-3 times greater following upward than downward tracking in all three subjects. A second approach to evaluating pursuit afternystagmus and its asymmetry involved a psychophysical test. A striking motion illusion develops if after a period of unidirectional tracking, the target is stopped and fixated. All of the eight subjects we tested reported that the target drifted in the opposite direction, initially quite rapidly but slowing down with time. The illusion seemed to be similar to a classical motion aftereffect. However, evidence has been presented (Chaudhuri 1990) that the motion illusion is generated by suppression of PAN. Specifically, in the presence of a fixation point during the afternystagmus period, the reflexive drift associated with PAN is believed to be offset by a pursuit signal in the opposite direction in order to maintain fixation. Eye movement records show a flat trace and total suppression of PAN in the presence of a fixation target. Chaudhuri (1990) proposed that the onset of retinal image motion of the fixation point by the PAN drift initiates and maintains an opposite pursuit signal and that the perceptual registration of the corollary discharge associated with this efferent motor signal generates the illusion. It was further shown that the velocity profile of the exponential decay of the illusion matched that of the PAN slow-phase drift. In this study, a directional asymmetry in illusory motion was reported by all eight subjects. The unequivocal impression of all subjects was that of a stronger motion illusion following upward tracking. As shown in Fig. 3b, the perceptual speed of the target, as obtained with the nulling technique, was significantly greater (/)<0.01; t-test, n = 5 ) at all points following upward
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pursuit than for downward pursuit. The same result was found in all three subjects. Furthermore, the total duration of the illusory motion was least following downward and highest following upward tracking in three subjects (Fig. 4). Discussion
Pursuit afternystagmus has been reported to have lower slow-phase velocities but similar time constants to OKAN (Muratore and Zee 1979). However, the only attempt at finding a directional asymmetry in the "direct" pathway produced mixed results (Murasugi and Howard 1989), The paradigm in that study was passive viewing of a moving random-dot field through a small central window. Subjects were instructed not to pursue individual features of the moving pattern. As a result, the OKN evoked by such restricted stimulation had a very low gain (0.11-0.28) and correspondingly, a weak OKAN. In the same study, stimulation of a larger strip of retina along the vertical meridian, however, produced a higher OKN gain and was sufficient to reveal the vertical OKAN asymmetry. Conditions that tend to reduce tracking gain, such as the presence of a low contrast textured background, also tend to reduce the afternystagmus and with it, muffle the asymmetry (personal observations). It would appear that the best means of examining asymmetries in the "direct" pathway is to use a smooth pursuit task and instruct subjects to actually track the moving target. At the stimulus velocities used in this study (7.5 deg/s), as well as the Murasugi/Howard study (30 deg/s), smooth pursuit gain is known to be considerably higher, and for the upward direction, very close to 1.0 (Baloh et al. 1986). We have found that such conditions not only produce an excellent pursuit afternystagmus but also reveal a striking anisotropy along the vertical axis. It has been suggested that the neural mechanisms underlying the ~ and "indirect" pathways are separate (Lisberger et al. 1981). The principle basis for this has been the dynamics of the two systems and the discharge characteristics of the velocity storage integrator. Although the finding that the smooth pursuit system also displays a slow discharge afternystagmus with a similar vertical asymmetry as the optokinetic system does not necessarily preclude the existence of separate mechanisms, since a small pursuit target may also weakly activate the "indirect" mechanism, the results reported here are consistent with the idea of a common velocityintegrator for both systems. If one of the sites of the velocity integrator is the vestibular nuclei, as has been suggested (Waespe and Henn 1977; Cannon and Robinson 1987), then the cortico-ponto-cerebellar pathway, which is believed to mediate smooth pursuit, could certainly have access to this mechanism since the principle efferents of the flocculus reach the vestibular nuclei (Carpenter and Cowie 1985; Langer et al. 1985b). Indeed, as of yet there are no known anatomical pathways by which the smooth pursuit system can influence the oculomotor nuclei directly and thus bypass the putative velocity storage sites.
475 The larger afternystagmus of the "indirect" pathway (Lisberger et al. 1981) may be a consequence of it being routed through an additional storage device. It is known from single-unit and lesion studies that the nucleus prepositus hypoglossi (NPH) is an important component of the "indirect" pathway and that it appears also to be a site of velocity integration (Luschei and Fuchs 1972; Keller 1974; Cheron et al. 1986; C a n n o n and Robinson 1987). The principle inputs to the N P H in the monkey are from other subcortical structures thought to be associated with O K N , such as the nucleus of the optic tract (Magnin and Baleydier, unpublished observations), mesencephalic reticular formation (Belknap and McCrea 1988), and the paramedian pontine reticular formation (Buttner-Ennever and Henn 1976). The oculomotor output of N P H units is then either channeled through the cerebellum and into the vestibular nuclei or directly to the vestibular nuclei (Langer et al. 1985a; Belknap and McCrea 1988). The dynamic properties of the "indirect" pathway may be a reflection of additional processing taking place within the N P H , a structure that is not an essential component of the "direct" pathway. This scheme is at present tentative and additional information on the anatomical and physiological properties of the two oculomotor pathways is required in order to fully understand the differences in their neural processing. The anisotropic nature o f smooth pursuit and O K N may be related either solely to the vestibular nuclei, upon which both pathways converge, or to velocity-storage integrators in general. Alternatively, the asymmetry may be a reflection of preferential processing along certain directions of motion at the input stage. Although there is some evidence to indicate this with regard to the "indirect" pathway (Mustari et al. 1988; Mustari and Fuchs 1989), there is no significant tendency to prefer motion along any particular direction in area M T (Albright et al. 1984), an extrastriate visual area in the monkey that appears specialized for motion processing which, along with other motion areas in the superior temporal sulcus, serves as an essential component of the "direct" pathway (Dursteler et al. 1987; K o m a t s u and Wurtz 1988). Thus, at present, the determinant of the oculomotor asymmetries expressed by both the "direct" and "indirect" pathways remains unknown. Acknowledgements. I thank Thomas Albright and Barry Frost for comments, and Frederick Nahm and Gene Stoner for participating in the eye-movement recording experiments. This work was supported by grant no. EY07605 from NIH. References
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