Abstract
Various research observations reported elsewhere are reviewed and interpreted here as they may be related in a process that is fundamental to the contralateral organization of the human nervous system. A functional explanation for the contralateral organization is theorized using these observations. It is proposed that, in response to the contralateral organization, conscious awareness is normally an illusory (right-left reversed) visual, auditory, tactile, and proprioceptive perception of external reality. Deviations from the normal functioning of the contralateral organization are thought to include right-left reversing goggle adaptation, the spoked-wheel illusion, and dyslexics who confuse alphabetic orientations. It is proposed that a theoretical right-left reversal memory process, which is separate from the contralateral organization, would further act to explain these phenomena.
It is remarkable that most of the ascending and descending sensorimotor communication tracts cross in either the medulla oblongata or the spinal cord. As a result of this crossing, nearly all of the sensory impulses received on one side of the body are perceived by the contralateral cortex. Moreover, fibers originating from one side of the cortex control primarily, if not entirely, muscle movements on the contralateral side of the body (Tortora & Derrickson, 2006). The adaptive advantage of the sensorimotor tracts crossing is unknown (Rodieck, 1998).
This article reviews and interprets various research observations reported elsewhere that, when considered together, may provide a functional explanation for the sensorimotor tracts crossing and the rest of the human nervous system's contralateral organization. The article is divided into four sections. The first section provides a background, an outline, and evidence for the contralateral organization theory presented here. A theoretical right-left reversal memory process that might explain kinesthetic and proprioceptive adaptation to right-left reversing goggles is described in the second section. The third section reviews evidence for the existence of right-left reversal of visual and non-visual spatial information in the human nervous system. In the fourth section, dyslexia is compared with the spoked-wheel illusion within the context of what is theorized here.
Sensorimotor organization and the cortical representation of the retinal image
The working assumption behind this article is that the human nervous system regularly reverses and inverts visual and non-visual spatial information about the external world. A necessary digression about perceptual plasticity is first provided in order to introduce concepts proposed here. Perceptual plasticity (flexibility) investigations often require subjects to wear, over several consecutive days, distortion goggles (optical devices containing lenses, prisms, or mirrors) that reverse or invert the retinal image. The brain does not change the cortical representation of the goggle retinal image to agree with the spatial properties that would otherwise be encoded from the normal retinal image. There is no compensatory change in visual perception with adaptation to distortion goggles. There is widespread agreement that adaptation to distortion goggles is entirely kinesthetic and proprioceptive (Harris, 1980; Linden, Kallenbach, Heinecke, Singer, & Goebel, 1999; Richter, Magnusson, Imamura, Fredrikson, Okura, Watanabe, et al., 2002). Kinesthesia refers here to the conscious perception of body position brought about by the directional movements and muscle tensions of the limbs and other body parts. Proprioception refers here to the unconscious perception of movement and spatial orientation arising from stimuli within the body itself.
The subjects' kinesthetic and proprioceptive perceptions of their arms, legs, and entire bodies feel reversed (and in agreement with what they see) after wearing right-left reversing goggles for an extensive period of time. Adaptation to the goggles becomes so complete subjects will write backward (from right to left) with the normally non-preferred hand. This motor activity feels normal, and subjects have stopped noticing that the letters and words still look reversed. The subjects' position sense also accurately adapts kinesthetically and proprioceptively to up-down inverting goggles (Harris, 1980). It is noted adaptation to up-down inverting goggles takes fewer days than with right-left reversing goggles (Livingston, 1978). It is thought up-down goggle adaptation would be shorter because of a proprioceptively learned memory representation cued by gravity. There is no apparent environmental cue such as gravity for distinguishing left and right. Right-left reversing goggles would possibly take more days, because adaptation to them would require choice using previously established right-left reversed memory representations (described in the second section of this article).
Precise information needed to make possible distortion goggle adaptation would be provided by specialized receptors in the muscles and joints called proprioceptors. They inform the brain about muscle and tendon tension, muscle stretch, and the angle between two bones connected by a joint (Rodieck, 1998). Other proprioceptors which would make possible adaptation with right-left reversal and up-down inversion include hair cells of the vestibular apparatus in the inner ear. They monitor head position during movements and the organization of the head in relation to the ground. Proprioceptors also convey the rate of movement of one body part in relation to others so we can walk, type, and dress without using our eyes (Tortora & Derrickson, 2006).
When the retinal image is reversed or inverted by distortion goggles, not only does body position sense adapt to it, but spatial location for sound also shifts in the direction of the altered visual sense. Visual capture of sound location occurs instantly, with little or no notice of intersensory discrepancy. This phenomenon is known as the ventriloquism effect (Howard & Templeton, 1966). However, this spatial plasticity is not considered to be adaptation because there is no change in auditory perception lasting beyond the visual exposure period (Welch, 1978). The explanation being proposed for this phenomenon relates to how the pathway for each ear is primarily connected to the contralateral cortex (Tortora & Derrickson, 2006).
It is not clear why there should be a potential for reversal and inversion of both body position sense and location of sound; perhaps the same things happen in the normal operation of kinesthetic and proprioceptive mechanisms as with distortion goggles. The lens of each eye, without distortion goggles, normally produces a right-left reversal and an up-down inversion upon each retina, appearing as an image on film in a camera would. When the eyes are fixated, the right visual field projects onto the nasal half of the retina of the right eye and the temporal half of the retina of the left eye. The axons from both of these hemiretinas terminate in the left occipital lobe so it processes the right visual field, and vice versa the right occipital lobe processes the left visual field. In conjunction with this, the upper half of the right visual field (or upper-right quadrant) is processed in the left occipital area below the calcarine sulcus and the lower half of the right visual field (or lower-right quadrant) is processed in the left occipital area above the calcarine sulcus and vice versa for the right occipital lobe and left visual field (Tortora & Derrickson, 2006). This outline implies the cortical representation of the field of vision is normally reversed and inverted (i.e., homologous with the normal retinal image).
To understand what is being proposed here, it is important to note the same functional topological pattern (contralateral organization) exists for what is visually experienced as for what is non-visually experienced. Suppose, then, one links the kinesthetic right-left reversal potential with the sensorimotor tracts crossing, considers the pathway for each ear is primarily connected to the contralateral cortex, and considers the evidence the cortical visual representation is homologous with the normal (right-left reversed) retinal image. These considerations carry the presumption that any intersensory organization capable of producing concurrent multimodal perceptual information about the same spatial event, presupposes separate underlying neurophysiologic mechanisms synchronized in a directionally related point-to-point correspondence. Cortical mapping of non-visual with visual information would seem most efficient in this way. Therefore, it is theorized that the sensory tracts crossing provides for a right-left reversal of non-visual spatial properties that become coded in concordance with the presumed right-left reversed spatial properties of the retino-cortical representation. Moreover, the motor tracts crossing brings about orientation and movement on each side of the body that veridically corresponds to external reality, although directionally reversed in relation to what the brain would consciously see, hear, and feel. The normal kinesthetic and proprioceptive actions would thus be directionally opposite of those observed with right-left reversing goggles—presuming the same perceptual motor model and contralateral pathways are followed in both instances. The logical implication of this would be a normal body position sense dependent upon an illusory (right-left reversed) visual, auditory, tactile, and proprioceptive sensory representation of external reality. People would not be aware of any part of this reversal because it is hypothesized that the motor tracts crossing right-left reverses the brain's motorical response pattern for the illusory perception to accurately match orientation and movement with external reality. The same thing would logically happen as observed with right-left reversing goggles. A proprioceptive memory representation of gravity, mentioned earlier, would separately act to accommodate the presumed up-down inverted spatial properties of the retino-cortical representation.
Right-left reversal of sensory memory
A theoretical construct called interhemispheric mirror-image reversal of sensory memory (c.f. Corballis & Beale, 1970, 1976, 1983, 1993; Corballis, 1974) might explain right-left reversing goggle adaptation. The Corballis and Beale interhemispheric reversal idea infers a property of plasticity which would occur in memory formation not in perception. According to them, both hemispheres would record the letter /b/ as a /b/ and would also register in memory a /d/ shape as well as the /b/. This potential for confusion would exist because the left and right visual fields appear to be mapped symmetrically in both hemispheres for integration across the vertical meridian of the visual cortical field. Corballis and Beale presume interhemispheric visual transfer processes must maintain mirror-image orientation because opposite sides of the meridian project mirror-image points in each opposite hemisphere (i.e., homotopically). They theorize that having these homotopic connections between the hemispheres would allow for the production of memory representations in both originally seen and right-left reversed forms. A person could then generalize from specific learned experiences in accordance with their right-left reversed memory representations. This symmetrization would enable recognition that an object can be oriented in different directions. It would also facilitate bilaterally symmetrical movements needed for many skills such as walking or swimming. Support for the Corballis and Beale idea comes from studies of optic-chiasm-sectioned monkeys. Monocularly trained to recognize asymmetrical visual objects, such monkeys respond preferentially to reversed images of the objects when viewed with the untrained eye (Noble, 1966, 1968).
Right-left reversals caused by interhemispheric transfer might explain why subjects can adapt to right-left reversing goggles so accurately. Because the reversals would be memorial they could establish pre-existing templates for recognition of perceptual inputs. For example, the goggles would make words appear right-left reversed, but if there are already memory representations corresponding to the reversed words, then adaptation should be facilitated. This might explain why subjects stop noticing that words still look reversed. The Corballis and Beale idea might also explain kinesthetic and proprioceptive adaptation to right-left reversing goggles. Subjects could use trial-and-error muscle movements to gradually adapt to pre-existing reversed motor memory representations. The world would begin to feel normal because the adapted motor information, in turn, would be used by subjects to gradually adapt to pre-existing reversed body position memory representations. Subjects having adapted to right-left goggle reversal would, upon removal of the goggles, use their original motor and body position memory representations (in the above mentioned kinesthetic and proprioceptive manner) to gradually resynchronize non-visual memory representations with normal visual input.
Right-left reversal in the human nervous system
Two well-known examples of right-left reversal of visual perception, without distortipn goggles, are stroboscopic presentations and spoked wheels turning in video frames which both at times appear to sporadically alternate clockwise and counterclockwise. Spoked-wheel illusions also occur in continuous light (i.e., in the absence of intermittent illumination). The continuous light illusions have been suggested as evidence the human nervous system processes motion by a series of temporally ordered events, as in moving picture frames (Purves, Payarfar, & Andrews, 1996; Andrews & Purves, 2005). Others have proposed a continuous flow of events that is unbroken (Kline, Holcombe, & Eagleman, 2004; Kline & Eagleman, 2008). The moving picture frame analogy best characterizes sensorimotor synchronization with the retino-cortical representation, as discussed in the fourth section of this article.
A well-known example of right-left reversal of motor movement, without distortion goggles, is mirror writing. Feinberg and Jones (1985) refer to 18 cases of mirror writing brought about by brain injury. All had left-hemisphere damage which caused backward writing (from right to left) with the left hand, suggesting reversals had occurred in the right hemisphere. Previously established reversed memory representations might explain their backward writing, if unilateral brain injury forced them to refer to the reversed representations. Gottfried, Sancar, and Chatterjee (2003) reported a more unique case of mirror writing. Their patient did not have a right hemiplegia as do most mirror writing patients, so her writing was tested with both hands. She wrote preferentially with both hands in the mirror direction, but produced normal appearing writing with more difficulty when using either hand. She also demonstrated an obvious preference for mirror reading. Gottfried, et al. interpreted her consistent mirror preferences as providing support for the Corballis and Beale idea of previously established memory representations corresponding to reversed words. According to Hécaen and de Ajuriaguerra (1964), 80% or more of most normal adults discover they can easily write backward with the non-preferred hand when asked to.
Evidence for the existence of a right-left reversal process being involved with visual memory is provided by a classic experiment performed by Standing, Conezio, and Haber (1970). They showed people 2,560 pictures of ordinary scenery for 10 seconds each, and when tested after three days, the subjects were able to achieve a high level of identification. What is noteworthy about their experiment is that right-left reversed photographic images, which had not been shown, were identified as often as the originals. In a similar vein, Rock (1973) describes an unpublished experiment by Olshansky in which people were shown novel shapes and then 2 minutes later tested for identification. Identification for right-left reversed images was almost that of the originals, but not similarly mistaken when the original images were inverted upside-down. False memory for inverted images would not be expected because memory for originally seen images would include up-down spatial information cued by gravity for proprioception. False memory for right-left reversed images would be expected if a right-left reversal process influences memory, as Corballis and Beale describe.
Dyslexia and the spoked-wheel illusion
Different types of eye movements (which include saccades and those involved in left-to-right scanning) may interact with an internal sense of direction when reading. These eye movements might always need to be completely synchronized with the corresponding, moving picture frame-like, retino-cortical representations for correctly distinguishing (i.e., remembering) originally seen from right-left reversed alphabetic memory representations. Proprioceptive cues would provide an internal sense of direction for remembering correct alphabetic memory representations and might possibly involve hand, foot, and eye dominance. This idea follows from the occurrence of dyslexic reading and writing reversals. Dyslexics (who confuse alphabetic orientations) have long been hypothesized as prone to a sensorimotor conflict between handedness and eye dominance (Orton, 1937; Harris, 1956). Additionally, dyslexics as a group show longer fixation durations, shorter saccade length, and a much larger number of regressions in comparison with non-dyslexic readers (Rayner, 1998). Furthermore, it has long been known that non-dyslexic children often find it difficult to establish the correct orientations for the letters of the alphabet when first learning to read and write. Their letters are sometimes written backward. Most noticeably, they fail to distinguish the mirror-opposite lowercase b from d and p from q (Davidson, 1935). Conceivably, then, an impaired or immature sensorimotor synchronization with the retino-cortical representation might leave the human nervous system directionally disoriented for remembering correct alphabetic orientations.
It is speculated that something similar to an impaired or immature sensorimotor synchronization with the retino-cortical representation might cause normal adults to visually perceive a reversal of spoked-wheel motion. A spoked wheel might appear to sporadically alternate clockwise and counterclockwise because visual image stabilization (which is thought to be provided by saccadic eye movements; Rodieck, 1998) would be weakened at the sensory level for visual motion synchronization. Accordingly, visual sensory memory for the presented frequency of spatial events (wheel rotations) would at certain motion speeds become unsynchronized with non-visual sensory memory for spatial events involving saccadic eye movements. The unsynchronized visual sensory memory output would arrive in conscious awareness as mixed sequences of originally seen and right-left reversed memory representations, which at times would spontaneously replace the proper directional motion of a spoked wheel with a reversal illusion. These motion speed processing irregularities would also cause a spoked wheel to appear to rotate more slowly than its proper rotation and at other times make it appear stationary. Unlike dyslexic reversals, normal adults would immediately be aware of any wheel motional irregularities.
Perhaps analogous with what is speculated here for spoked-wheel motion, visual motion processing has been linked to reading level (Eden, Brown, Jones, Given & Zeffiro, 2000; Eden, Van Meter, Rumsey, Maisog, Woods, & Zeffiro, 1996) and visual motion sensitivity has been linked to orthographic skill (Talcott, Witton, McLean, Hansen, Rees, Green, et al., 2000; Talcott, Gram, Van Ingelghem, Witton, Stein, Toennessen, et al., 2003). Therefore, various eye movements might always need to be completely synchronized with the corresponding retino-cortical representations for correctly distinguishing originally seen from right-left reversed alphabetic memory representations when reading and writing.