Ординатура / Офтальмология / Английские материалы / Oculomotor Systems and Perception_Ebenholtz_2001

The Otolith–Ocular Reflexes 69

Gravitational

force

Kinocilium

Stereocilia

Otolithic membrane

Efferent nerve supply

Afferent output

to Vestibular

nucleus

Figure 3.19. The Equivalence of Linear Translation and Head Tilt. A stylized cross section of a hair cell mechanism with only four stereocilia are shown whereas actually more than 50 hairs per cell are common. Imagine the hair cells distributed over the sacculi and utriculi with the hairs perpendicular to the pictorial planes, whereas the otoconial layer, containing the calcium carbonate crystals, is parallel to this plane. If the hair cell is rotated clockwise so that gravitational force acts along the otoliths, this force is transmitted through the otolithic membrane to the kinocilium and the distal tips of the hair bundle to produce an increased afferent output. A force acting away from the kinocilium [to the left in Fig. 3.19] causes hyperpolarization, a reduced response, whereas intermediate angles yield output proportional to the cosine of the force angle (Hudspeth, 1983). These organs probably encode head position relative to gravity and signal antigravity muscle reflexes and oculomotor responses such as torsion and the doll reflex (see Fig. 3.20 and Chapter 4).

It is significant that a constant linear acceleration to the left because of the greater inertial lag of the otoliths in relation to the hair bundle displaces the stereocilia toward the right, thereby increasing afferent output. Thus, in the example given, a clockwise tilt in a gravitational field and a linear acceleration to the left may, in principle, produce identical afferent neural output. This equivalence may have been at the root of airplane disasters when aircraft carrier pilots, on accelerating at take-off, felt they were excessively pitched upward. Correction from this illusory attitude promptly caused an irrecoverable dive into the ocean (Cohen, Crosbie, & Blackburn, 1973).

70 Oculomotor Systems

down,onlyabout9degofcompensatoryeyerotationmaybeexpected(Bucher, Mast, & Bischof, 1992). This low gain indicates that the torsional reflex is barely functional. Consistent with expectations from the equivalence of otolithic stimulation due to left or right head tilt and lateral translation, human torsional eye movements have been observed and measured during linear oscillation along the interaural (left–right) axis (Lichtenberg, Young, & Arrott, 1982), where they certainly cannot contribute to gaze or image stability.

As one might expect from an oculomotor system driven by mechanisms sensitive to gravito-inertial forces, the torsional positions of the two eyes depart from their normal 1-g positions during the 0-g phase of parabolic flight (Money et al., 1987). In what has become a conventional procedure, NASA researchers typically use a KC-135 aircraft as a flying laboratory. To achieve a 0-g state, the pilot approximates a parabolic trajectory, at the peak of which, the aircraft pitches downward and enters a brief period (about 25 s) of free fall. The aircraft then gradually pitches upward and accelerates, thereby increasing gravito-inertial force, to achieve about 25 s of 1.8-g , then decelerating until the peak of the parabola is reached. The process usually is repeated about 20 times on the outward bound leg and again 20 times on the return portion of the trip. Nausea and emesis are frequent-flyer rewards on these flights.

Because the 0-g state characterizes the space environment of astronauts (see later, the discussion of adaptation in space), it is most likely that similar ocular torsional displacements also occur in earth orbit, where it is thought that they contribute to space motion sickness (Diamond & Markham, 1991). Accordingly, it may not be mere coincidence that, when Balliet and Nakayama (1978) succeeded in training their earthbound subjects to produce voluntary torsion, which, surprisingly, yielded rotational amplitudes as high as 30 deg, subjects experienced nausea and other motion sickness symptoms. (See Chapter 5 for a further discussion of the role of ocular muscle traction in motion sickness.)

Finally, it is worth noting that torsion may thus join accommodation as members of a class of ocular reflexes that, with proper feedback, may be placed under voluntary control.

In a fashion somewhat analogous to ocular counterrolling, when the head is pitched back, as when looking up, or when the whole body is pitched back in a supine posture, the downward acting ocular muscles are stimulated reflexively, similar to the movement of counterweighted doll eyes. This produces a bias in the position of the eyes that the subject believes to represent a straight ahead gaze (i.e., the subjective straight-ahead eye position shifts downward with backward pitch; Ebenholtz & Shebilske, 1975; Citek & Ebenholtz, 1996). Peak shift with backward tilt occurs around 90 deg of pitch, as shown in Fig. 3.20, and

72 Oculomotor Systems

is under about 10 deg; therefore of the same order of magnitude as the counterrolling reflex. Likewise, linear acceleration in the naso-occipital direction (straight ahead or backward with head upright) induces vertical responses that are nonfunctional at low frequencies of oscillation (0.5 Hz, Paige & Tomko, 1991a,b). In the latter study, their subjects (squirrel monkeys) showed signs of a remarkable oculomotor mechanism, a gaze-dependent compensatory response. They found, for example, that during forward movement in darkness when initial gaze direction was straight ahead, no response was made, whereas when initially gazing to the left, a further leftward response occurred, and likewise the eye rotated rightward during right gaze and upward or downward duringupanddowngazes,respectively. Theconvergenceangleandeccentricity of initial gaze also heavily influenced the subsequent response. No comparable data are currently available on humans, nor is it known what influence the immobilization of the head had on these responses. Nevertheless, given the strong conditional nature of these oculomotor responses, it seems likely that they were shaped by the optic flow patterns to produce functionally valid linear vestibulo-ocular reflexes (LVOR) conditional on initial gaze direction. Such conditional changes have indeed been demonstrated in the case of the gain of the horizontal VOR associated with up and down gaze (Shelhamer, Robinson, & Tan, 1992).

Otolith–Ocular Adaptation in Outer Space

In order to consider how the otolith–ocular reflexes behave in outer space, it is important to note that the distance from Earth to an orbiting space ship, about 300 miles, is much too short to reduce the force of gravity by more than about 15 percent. Nevertheless, the gravito-inertial force on astronauts is effectively zero because they are in a condition of perpetual free fall, owing to the balance achieved by the centripetal g -force and the tangential acceleration that maintains ship and crew in circular orbit. Because all objects, regardless of mass, fall at the same rate in a gravitational field, the hair cells of the otolith organs are not affected by the overlying otoliths, regardless of head angle assumed. Thus, with head tilt, as far as signals from the utricle and saccule are concerned, except for the spontaneous, resting-level neural output and response to linear acceleration, the brain in space orbit is essentially deafferented, as though the otolith-organ portion of the eighth nerve had been cut, while sparing the signals from semicircular canals. A similar unloading of the utriculi (but not the sacculi) occurs when upside down on Earth, and may be related to the frequent reports of subjective inversion by astronauts in

An Overview of Oculomotor Systems 73

orbit (Kerwin, 1977) and in the zero-g phase of parabolic flight (Graybiel & Kellogg, 1967). Under these conditions, apparent body orientation is heavily influenced by vision and proprioception (Lackner & Graybiel, 1983).

As noted previously, although otolith organs do not respond to head tilt in space orbit, they do respond to linear acceleration. This arises out of the special type of human locomotion required in space. Here, walking is not possible. Instead, one is launched into space each time the toe pushes off. Hence, astronauts tend to glide and dive (glive?) toward their destination. These sequences of transitional acceleration and deceleration trigger transient otolith activity much more frequently than is the case on Earth. The combination of an optic array signalling translation together with otolith activity may be a sufficient adaptive stimulus for a change both in the central interpretation of otolith stimulation and in the type of eye movement normally triggered. This has been termed the tilt-translation reinterpretation hypothesis (Young et al., 1984; Parker et al., 1985). Accordingly, one finds on return to Earth reports by astronauts that head tilt elicits a sense of vection with translational components (Parker et al., 1985), and many reports of a reduction in ocular counterrolling after space flight (e.g., Vogel & Kass, 1986; Dai et al., 1994). Thus, it appears as though the adaptive neural networks of the vestibular cerebellum are extremely active in outer space.

An Overview of Oculomotor Systems

Categories of Oculomotor Function

A wide variety of interesting ways are available by which to categorize and study eye movements, including ontogenetic (Aslin & Dumais, 1980) and phylogenetic (Walls, 1962; Hughes, 1977) approaches. A different but equally pragmatic set of categories is represented in Table 3.00 according to nominal stimulus conditions and apparent visual function. The classification may have some heuristic pedagogic value, but it is not perfect because many system attributes actually are shared. For example, typical saccades occur during the quick phases of VOR and OKR (Ron et al., 1972); saccades play a significant role in asymmetric vergence (Enright, 1992); and slow drifting eye movement, not just saccades, can be used to maintain foveation (Steinman, Cunitz, Timberlake, & Herman, 1967). These and many other observations provide ample evidence for the extensive sharing of structure and function across the various oculomotor systems. The present piecemeal approach reflects a convenience of analytic research, soon to give way to more integrative studies

74 Oculomotor Systems

Table 3.00. Oculomotor systems grouped by stimulus condition and primary function

reflecting system interactions. For example, Schor, Lott, Pope, and Graham (1999) investigated saccades that occur immediately after a blur stimulus and found them to reduce the latency of focusing and increase the speed of both accommodation and accommodative vergence. Likewise, saccades have been shown to facilitate changes in disparity vergence (Enright, 1984). Thus, the next phase of research has already begun.

78 Oculomotor Factors in Perception

γ

φ

α

Figure 4.00. A System of Egocentric Angular Coordinates. (From Ebenholtz, 1984, Perceptual coding and adaptations of the oculomotor systems. In L. Spillman

&B. R. Wooten (Eds.), Sensory experience, adaptation, and perception: Festschrift for Ivo Kohler, Chap. 19. Reprinted by permission of Lawrence Erlbaum Associates, Inc.) The convergence angle γ encodes distance, whereas the angles α and φ encode elevation and horizontal orientation, respectively. The latter derive from the version or conjugate system of eye movements. When the eye does not fixate the target of interest, its egocentric orientation may nevertheless be registered provided that (1) eye position in the head is known, and (2) the angular deviation of the target image relative to the fovea also is known (Morgan, 1978).

Sensing the location of an object in relation to some part of the self is a precursor for action. One may then direct the hands toward it, walk toward or runaway from its locus, direct one’s voice properly, or otherwise send signals toward the object. Thus, egocentric localization is of central importance for animal (and robot) behavior, and therefore it would not be surprising to find redundant systems evolved for the task of spatial orientation. Although psychologists have devoted a great deal of intellectual effort to devise theories of how the dynamic image on the retina of a moving observer may encode orientation information (Gibson, 1966; Hildreth, 1992; Perrone, 1992), research supports the integration of this approach with a corresponding role for oculomotor systems (Royden, Crowell,

&Banks, 1994; Bradley et al., 1996).

shown in Fig. 4.00 and the point between the eyes from which the world is perceived (Fig. 4.01). These ideas were developed by Hering (1879/1942) and expressed in the notion of a hypothetical cyclopean eye, as shown in Fig. 4.01(c and d).

The principle represented in Fig. 4.01(d) is that eye position must be registered in the brain in order to associate an egocentric direction with any particular point in a retinal image. One implication of this fact is that the pattern of brain stimulation produced by a retinal image is thoroughly ambiguous