Egocentric perception through interaction among many sensory systems
Introduction
We move around to maintain our everyday life. When we move, we sense not only whether we are moving or not, but also the speed and direction of our own motion. It has been known that many sensory systems contribute to the sensation of self-motion. The primary system for sensation of self-motion is the vestibular system, a set of sensory organs within the inner ear on each side of the head. These organs evolved from primitive sensory organs consisting of cells covered with sensitive hairs in fluid-filled holes in the skin. There are three canals and two otolith organs in our vestibular system. The canals are sensitive to rotation of the head and the otolith organs sense gravity and linear acceleration of the head [1].
Each canal is a complete fluid circuit and at one point there is a swelling, or ampulla, which contains sensory hair cells. The force by the rotation of the head causes the fluid to circulate relative to the wall of the canal in a direction opposite to the force. The circulation of fluid stimulates the sensory hair cells through deflection of a gelatinous mass, or cupula in the ampulla. The relationship between the angular acceleration of the head and the angular displacement of the cupula is described by the second-order differential equation with three coefficients, namely the elasticity (position-dependent resistance), the viscosity (velocity-dependent resistance) and the moment of inertia (mass-dependent resistance) of the cupula and the fluid. Since the elasticity and the moment of inertia are small compared with the viscosity, the angular velocity of displacement of the cupula is approximately proportional to the angular acceleration of the head. If this relation is integrated with time, the displacement of the cupula is proportional to the angular velocity of the head. Therefore the canal is an integrating angular accelerometer for the head rotation. Although the response of the canal becomes proportional to the acceleration of the head for slow rotation, the canal works as an angular speedometer as long as the velocities of head rotation are high enough [2]. However, since the canal is stimulated by the angular acceleration rather than the angular velocity of the head, it ceases responding to prolonged head rotation with constant angular velocity.
The three vestibular canals (the horizontal canal, the posterior vertical canal and the anterior vertical canal) are specialized for different axes of head rotation. Since the horizontal canal is not aligned with the horizontal plane of the head and the three canals are not arranged at right angles, each canal is not necessary tuned to yaw, pitch and roll of the head. Any rotation of head creates patterns of stimulation in all three canals [3].
The otolith organs (the utricle and the saccule) are sack-shaped cavities at the junction of the three canals. The cavity is filled with fluid and contains sensory hair cells that are covered with a gelatinous substance containing calcite crystals (the otoliths). The hair cells respond to displacement of the heavy otoliths caused by changes of the linear acceleration of the head. Changes in the linear velocity of the head or in the direction of the head motion bring changes in the linear acceleration of the head. A tilt of the head with respect to gravity also brings changes in the linear acceleration of the head. Therefore the otolith organs are stimulated by a linear acceleration of head motion as well as by tilting of the head, and resulting responses are not distinguishable. One well-known consequence of this fundamental ambiguity is the experience of pilots when an aircraft increases speed. The otolith organs are stimulated in the same way as when there is upward pitch of the aircraft. If there is no other information available, the pilot may bring the nose down to correct the aircraft and fly it into the ground [4].
When we are actively moving, the somatosensory system as well as the vestibular system contributes to the sensation of self-motion. Information from proprioceptors at the neck and other joints, from foot mechanoreceptors and sensorimotor feedback from the legs and trunk, bring the sensation of self-motion [5]. Although it was reported that the somatosensory information from muscle and joint receptors induced a sufficient amount of sensation about speed of self-motion, the role of the somatosensory system in perceived direction of self-motion has not been examined.
The third but not the least important sensory system contributing to the sensation of self-motion is the visual system. The sensation of self-motion induced by visual stimulation is a phenomenon that occurs in everyday life [6]. When a neighboring train pulls away, we experience the stationary train in which we are seated to be moving in the opposite direction [7]. The visually induced sensation of self-rotation is called as circular vection and the visually induced sensation of self-translation is called as linear vection [8]. The induced sensations of body motion are not distinguishable from sensations caused by actual motions of the body. This suggests that there is a common neural mechanism for the sensation of self-motion that receives information both from the visual system and from the vestibular system [9].
The vection is sometimes described as the visually induced illusion of self-motion. Although this seems to make sense because we feel our own motion by the visual stimulation while we are not moving, it could be a misnomer to call the vection an illusion. After a prolonged period of passive motion of the body at a constant speed for about 30 seconds, the vestibular system returns to the resting state and ceases to respond [10]. The only indication of self-motion is countermoving visual surroundings. Naturally visual surroundings do not move unless the body moves, so when they are perceived to be moving relative to the self, the best bet is that the motion is due to self-motion. Therefore, it is not surprising that a large moving display induces the most convincing sensation of self-motion. It is the natural cue for the self-motion.
It was reported that the circular vection around the yaw axis (the yaw vection) decreased significantly when the central part of visual field less than 60° diameter was stimulated [10]. On the other hand the linear vection along the line of sight (the forward vection) did not decrease significantly even when the visual stimulus was presented on the central visual field of only 5° diameter [11]. The discrepancy about the effect of the field size of the visual stimulus on the vection suggests that characteristics of interaction between the canal and the visual system are different from those between the otolith and the visual system. The visual displays for these two directions of vection were quite different, too. The visual display for the yaw vection was a lamellar movement of the vertical bars in the horizontal direction, and the display for the forward vection was a looming, or radically expanding, randomly-spaced-dots pattern [12]. The discrepancy about the size effect could be due to the result of different processing mechanism for these displays in the visual system.
It was reported that both the yaw vection and the forward vection were governed by the motion of the display that was perceived to be the more distant one 13, 14, 15. These results make sense ecologically. Since more distant objects are unlikely to move with the person, their movement relative to the head provides a more reliable indicator of self-motion than does the motion of nearer objects, which might be attached to, and therefore move with, the person. However, the inhibitory effect of a stationary background on the forward vection was weaker than that found with the yaw vection. This difference makes sense because, for forward body motion, the image on a distant scene is virtually stationary whereas, when the body rotates, it is not.
It seems to be a general rule that the vection is induced best by the visual stimulus presented on the retinal periphery and as the background. When these two visual factors were combined, the retinal periphery was dominant for inducing the yaw vection except when the moving central display was presented behind the stationary peripheral display. The observers who perceived the moving central display through a stationary window reported sufficient vection, and the other observers who did not see the peripheral display as a window did not report vection [16]. This suggests some higher-level control on induction of the vection.
The sensation of self-motion is achieved either by the vestibular system, by the somatosensory system or by the visual system. When we move around in the real world, all these three senses simultaneously contribute to the sensation of self-motion. However, there has not been enough research on understanding how the sensory signals from these different mechanisms are combined. One reason for this is that the measurement of vection relies on a subjective method of magnitude estimation, and it is difficult to analyze the experimental data quantitatively.
In the first experiment of this report, we used perceived direction rather than perceived speed as a measure of the sensation of self-motion, and investigated the interaction between the vestibular information, the somatosensory information and the visual information. In the second experiment, we chose the body sway accompanying the sensation of self-motion as a measure, and investigated the contribution of the visual system on the body sway when the visual display consisted of two axes of linear acceleration.
Section snippets
Experiment 1
The visual system is an ideal heading detector, since it consists of spatially discrete neurons sensitive to the velocity and direction of optical flow resulting from the relative motion of stationary objects in the environment. Gibson noted that direction of heading is specified by the centre of radial optical flow, that is, the `focus of expansion' [17]. However, the focus of expansion is useful only when an observer is following a straight path while keeping the gaze on the direction of
Experiment 2
It has been reported that when erect observers watch a moving display, their body sways to the same direction as the motion of display. On the other hand, the direction of visually induced perception of self-motion is to the opposite direction of the visual display. Therefore, it is a general understanding that the body sway occurs to keep the posture vertical against perceived body sway accompanying with the visually induced sensation of self-motion.
The reported characteristics of the visually
Discussion
The results of the first part of Expt. 1 showed that perception of the direction of self-motion was reasonably accurate and precise during combined visual-somatosensory stimulation when observers moved at subthreshold accelerations. This means that observers do not necessarily need the vestibular input for the judgment of direction of heading. The vestibular system may contribute to the perception of the direction of self-motion during the acceleration phase of self-motion, or when visual
Acknowledgements
Experiment 1 of this research was done with Drs. Laura Telford and Ian P. Howard at Centre for Vision Research, York University with support by a grant from the National Science and Engineering Research Council of Canada. Experiment 2 was done with Dr. Tatsuya Yoshizawa at MATTO Laboratories, Kanazawa Institute of Technology with support by a grant from the Ministry of Science and Technology of Japan.
References (40)
- Howard, I.P., Human Visual Orientation, John Wiley & Sons, Chichester, 1982, pp....
- Melvill Jones, G., The vestibular system for eye movement control. In R.A. Monty and J.W. Senders (Eds.), Eye Movements...
- Branks, R.H.I., Curthoys, I.S. and Markham, C.H., Planar relationships of semicircular canals in man, Acta...
- Wolfe, J.W. and Cramer, R.L., Illusions of pitch induced by centrifugal acceleration, Aerosp. Med., 41 (1970)...
- Walsh, E.G., Role of the vestibular apparatus in the perception of motion on a parallel swing, J. Physiol. (Lond.), 155...
- Wood, R.W., The `haunted-swing' illusion, Psychol. Rev., 2 (1895)...
- Duncker, K., Ueber induzierte Bewegung, Psychol. Forsch., 22 (1929)...
- Fischer, M.H. and Kornmüller, A.E., Optokinetisch ausgelöste Bewegungswahrnehmung und optokinetischer Nystagmus, J....
- Dichgans, J. and Brandt, T., Optokinetic motion sickness and pseudo-Coriolis effects induced by moving visual stimuli,...
- Brandt, T., Dichgans, J. and Koenig, E., Differential effects of central versus peripheral vision on egocentric and...
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