Brain, Vol. 123, No. 7, 1293-1326,
July 2000
© 2000 Oxford University Press
Invited review |
Cerebral specialization and interhemispheric communication
Does the corpus callosum enable the human condition?
Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire, USA
Correspondence to:
Michael S. Gazzaniga, Center for Cognitive Neuroscience, Dartmouth College, Hanover, NH 03755, USA
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Abstract |
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 Top Abstract IntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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The surgical disconnection of the cerebral hemispheres creates an extraordinary opportunity to study basic neurological mechanisms: the organization of the sensory and motors systems, the cortical representation of the perceptual and cognitive processes, the lateralization of function, and, perhaps most importantly, how the divided brain yields clues to the nature of conscious experience. Studies of split-brain patients over the last 40 years have resulted in numerous insights into the processes of perception, attention, memory, language and reasoning abilities. When the constellation of findings is considered as a whole, one sees the cortical arena as a patchwork of specialized processes. When this is considered in the light of new studies on the lateralization of functions, it becomes reasonable to suppose that the corpus callosum has enabled the development of the many specialized systems by allowing the reworking of existing cortical areas while preserving existing functions. Thus, while language emerged in the left hemisphere at the cost of pre-existing perceptual systems, the critical features of the bilaterally present perceptual system were spared in the opposite half-brain. By having the callosum serve as the great communication link between redundant systems, a pre-existing system could be jettisoned as new functions developed in one hemisphere, while the other hemisphere could continue to perform the previous functions for both half-brains. Split-brain studies have also revealed the complex mosaic of mental processes that participate in human cognition. And yet, even though each cerebral hemisphere has its own set of capacities, with the left hemisphere specialized for language and speech and major problem-solving capacities and the right hemisphere specialized for tasks such as facial recognition and attentional monitoring, we all have the subjective experience of feeling totally integrated. Indeed, even though many of these functions have an automatic quality to them and are carried out by the brain prior to our conscious awareness of them, our subjective belief and feeling is that we are in charge of our actions. These phenomena appear to be related to our left hemisphere's interpreter, a device that allows us to construct theories about the relationship between perceived events, actions and feelings.
cerebral specialization; callosum; interhemispheric; interpreter
HERA = hemispheric encoding/retrieval asymmetry; LVF = left visual field; RVF = right visual field; SOA = stimulus-onset asynchrony
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Introduction |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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In the pages of this journal much of the original work on disconnection syndromes has been described, especially the effects of surgical section on the corpus callosum. Over 30 years ago, Norman Geschwind's magnificent two-part review article on disconnection syndromes (Geschwind, 1965a
, b) launched not only a thousand research ships but provided the intellectual basis for a new behavioural neurology, particularly in the USA. In what follows I review progress in studying patients with surgical disconnection of the cerebral hemispheres. I concentrate on research over the past 40 years, especially as it relates to current views of the human brain's neurological organization. This work is of a particular kind in that each cerebral hemisphere is examined with the help of specialized stimulus lateralization techniques. These techniques have evolved over years of testing and they allow unique ways of interpreting the neuropsychological assessment of these surgical cases. As a consequence, studies that do not use these testing procedures are limited and will not be reviewed. |
General background |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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The human brain is a bizarre device, set in place through natural selection for one main purpose—to make decisions that enhance reproductive success. That simple fact has many consequences and is at the heart of evolutionary biology. Once grasped, it helps the brain scientist to understand a major phenomenon of human brain function—its ubiquitous lateral cerebral specialization. Nowhere in the animal kingdom is there such rampant specialization of function. Why is this, and how did it come about?
What emerges from split-brain research is a possible insight to these questions. It may turn out that the oft-ignored corpus callosum, a fibre tract that is thought merely to exchange information between the two hemispheres, was the great enabler for establishing the human condition. Non-human brains, by contrast, reveal scant evidence for lateral specialization, except as rarely noted, for example, by Hamilton and Vermeire while they were investigating the macaque monkey's ability to perceive faces (Hamilton and Vermeire, 1988). In that study, they discovered a right hemisphere superiority for the detection of monkey faces.
With the growing demand for cortical space, perhaps the forces of natural selection began to modify one hemisphere but not the other. Since the callosum exchanges information between the two hemispheres, mutational events could occur in one lateralized cortical area and leave the other mutation-free, thus continuing to provide the cortical function from the homologous area to the entire cognitive system. As these new functions develop, cortical regions that had been dedicated to other functions are likely to be co-opted. Because these functions are still supported by the other hemisphere, there is no overall loss of function. In short, the callosum allowed a no-cost extension; cortical capacity could expand by reducing redundancy and extending its space for new cortical zones.
This proposal is offered against a backdrop of new findings in cognitive neuroscience, findings that strongly suggest how important local, short connections are for the proper maintenance and functioning of neural circuits (Cherniak, 1994; Allman, 1999). Long fibre systems are relevant—most likely for communicating the products of a computation—but short fibres are crucial for producing the computation in question. Does this mean that as the computational needs for specialization increase there is pressure to sustain mutations that alter circuits close to a nascent site of activity?
One of the major facts emerging from split-brain research is that the left hemisphere has marked limitations in perceptual functions and that the right hemisphere has even more prominent limitations in its cognitive functions. The model thus maintains that lateral specialization reflects the emergence of new skills and the retention of others. Natural selection allowed this odd state of affairs because the callosum integrated these developments in a functional system that only got better as a decision-making device.
Another aspect of this proposal can be seen when considering possible costs to the right hemisphere. It now appears that the developing child and the rhesus monkey have similar cognitive abilities (Hauser and Carey, 1998). It has been shown that many simple mental capacities, such as classification tasks, are possible in the monkey and in the 12-month-old child. Yet many of these capacities are not evident in the right hemisphere of a split-brain subject (Funnell and Gazzaniga, 2000). It is as if the right hemisphere's attention–perception system has co-opted these capacities, just as the emerging language systems in the left hemisphere co-opt its capacity for perception.
With these changes ongoing, one might predict that there would be an increase in local intrahemispheric circuitry and a reduced interhemispheric circuitry. With local circuits becoming specialized and optimized for particular functions, the formerly bilateral brain need no longer keep identical processing systems tied together for all aspects of information processing. The communication that occurs between the two hemispheres can be reduced, as only the products of the processing centres need be communicated to the opposite half-brain. Recently, Rilling and Insel have reported that there is a differential expansion of cerebral white matter relative to the corpus callosum in primates (Rilling and Insel, 1999). Humans show a marked decrease in the rate of growth of the corpus callosum compared with intrahemispheric comparisons of white matter.
There is also new evidence that could lead the way to discovering how new functions, exclusively human in nature, arise during cortical evolution. Neurons in the monkey's prefrontal lobe respond not only when the animal is going to grasp a piece of food but also when the human experimenter is about to grasp the same piece of food (Rizzolatti et al., 1996). It would appear that circuits in the monkey brain make it possible for the monkey to represent the actions of others. Rizzolatti (Rizzolatti, 1998) suggested that such a system might be the seed for the uniquely human theory of a mind module (Baron-Cohen, 1995).
It is against this backdrop—one in which developmental and evolutionary time come into play and a dynamic cortical system establishes adaptations that become laterally specialized systems—that I review research on hemispheric disconnection syndromes. First, I examine basic neurological systems related to the senses, and then I consider issues in motor control. The evolutionary perspective creeps in early as we see similarities and differences in organization between the monkey and human visual systems. Building on these aspects, I survey perceptual and cognitive issues that have been studied intensely over the past 35 years, and I present them from an evolutionary perspective as well.
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Patient population |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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Over the years, two major patient populations have been investigated in split-brain studies. The first surgical series originated with Bogen and colleagues in California (Bogen et al., 1965
). These patients purportedly had their corpus callosum and anterior commissure sectioned in one operation. The case histories of the most frequently studied patients have been reported elsewhere and include the history of patients L.B., N.G., A.A., N.Y., C.C. and N.W. A 20-year follow-up MRI of these six patients confirmed the callosal section but not the section of the anterior commissure (Bogen et al., 1988).
The second surgical series was undertaken at Dartmouth Medical School by Donald Wilson and David W. Roberts (e.g. Wilson et al., 1977). This series included several patients who have been studied extensively, including patients P.S., J.W., and D.R. Another patient has been patient V.P., who was operated on by Dr Mark Rayport at the Medical College of Ohio. Finally a new patient, V.J., was operated on in California by Stephen Nudik. She had a post-operative MRI and the entire callosum had been successfully sectioned (Baynes et al., 1998). Extensive clinical histories for most of the foregoing patients have been reported elsewhere (Gazzaniga et al., 1984).
The studies reported below make use of all of these patients. Most experiments report results in which at least two of the patients reported above were examined. Overall, it can be said that the broad description of the split-brain syndrome applies to all patients who have undergone either full callosal surgery or section of the forebrain commissure. In what follows, experiments that bring out differences in performance between patients note which patients are being characterized.
Finally, the large literature on callosal agenesis is not reviewed. Massive brain reorganization takes place in these patients, and while some deficits of interhemispheric transfer on some limited tests have been observed (Aglioti et al., 1993; Lassonde et al., 1995), they show few of the dramatic deficits that occur following surgical section of the corpus callosum (Jeeves and Silver, 1988).
Methodological approaches
Over the years, several methodological advances have improved the perceptual and cognitive testing of patients who have undergone commissurotomy. In the original testing, mechanical timing devices were used to back-project 35 mm slides tachistoscopically. In more recent times, computer-driven stimulus presentation systems have been used. Throughout the progression of research, new technologies have given a boost to testing perceptual and cognitive aspects of the two separated or partially separated hemispheres (Fig. 1).
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Basic neurological mechanisms |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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For sensory systems, dramatic similarities and differences are evident in how the subhuman primate and human visual system are organized. The simple and compelling fact is that the two systems contrast significantly with each other. These differences may reflect an overarching principle of brain evolution: cortical space is co-opted for new purposes.
With the remarkable separation of sensory information and with the lateralization of corticospinal motor systems, the split-brain animal and human raise interesting questions about the neural mechanism by which motor activities occur. In particular, in recent years, these patients have provided the opportunity to test theories about the nature of the neural pathways that coordinate hands and arms. As we know, the ability to manipulate the environment reached a pinnacle when the fully opposable thumb evolved in humans. Not surprisingly, the brain contains specialized circuitry to exploit this capacity for prehension. In what follows, I examine the relevant sensory and motor research.
The anterior commissure does not transfer visual information in the human but does in the monkey
A major difference between the visual system of monkey and human is that the intact anterior commissure in the monkey transfers visual information of all kinds (Gazzaniga, 1966) (Fig. 2). The intact human anterior commissure appears to transfer nothing visual (Seymour et al., 1994; Gazzaniga et al., 1965; Funnell et al., 2000a, b). The fact that visual information remains lateralized to one hemisphere after callosal section in humans was first demonstrated by using quick-flash tachistoscopic presentation methods. It was clear that visual information presented to the right visual field projected exclusively to the left hemisphere and information presented to the left visual field projected exclusively to the right hemisphere. These observations have now been confirmed by employing prolonged stimulation with the Purkinje eyetracker and image stabilizer (Gazzaniga et al., 1996).
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One possible explanation for the differences between the visual systems of the two species can be found in the manner in which the visual system developed in humans. It is now known that the cortical fields of origin for neurons of the anterior commissure fibres are extensive in the monkey and reach far into the temporal lobe. By contrast, the projection fields of these neurons are more limited and include only the anterior third of the temporal lobe (Zeki, 1973
; Jouandet and Gazzaniga, 1979). While the pattern of projections is not known for the human, it is interesting to speculate that the caudal projections through the anterior commissure were crowded out by the addition of specialized regions that developed in the anterior regions of the visual system. This left the anterior commissure for olfactory and non-visual communication. Regions involved in early stages of visual processing would remain unaffected by the addition of these new functional regions. This is consistent with the view that there are no major interspecies differences in the early stages of the visual system.
Humans have visual midline overlap phenomena
Nasotemporal overlap at the retinal vertical meridian in cat and monkey is readily evident (Stone, 1966; Stone et al., 1973; Bunt and Minkler, 1977; Leventhal et al., 1988). In a 1–2° stripe that straddles the two visual half-fields, visual information is sent to the left and right visual cortices. Whether the anatomical projections have any functional significance has never been established, but there has been speculation that this zone might be responsible for the phenomenon of `macular sparing' (Bunt and Minkler, 1977; Leventhal et al., 1988). Strokes affecting the primary visual cortex in either hemisphere produce blindness in the opposing visual field, but within the blind field a small region of central vision is frequently preserved. Sparing can be explained by the assumption that, because of nasotemporal overlap, the entire fovea is represented in both hemispheres. By contrast, in neurologically normal subjects, attempts to demonstrate this zone psychophysically have failed consistently (e.g. Harvey, 1978; Lines and Milner, 1983). Fendrich and colleagues have examined this in split-brain subjects (Fendrich and Gazzaniga, 1989; Fendrich et al., 1994). Using an image stabilizer in combination with a Purkinje eyetracker, careful assessment of the visual midline of two split-brain patients has revealed an area no more than 2° wide at the veridical midline where some visual information appears available to each half-brain (Fig. 3). This contrasts with the findings of Sugishita and colleagues, who found no evidence of overlap in hemianopic subjects but did not have the advantage of image stabilization and were restricted to only brief stimulus presentations (Sugushita et al., 1994). The strip of overlap does not encompass the entire fovea. Within this strip the signals conveyed to each hemisphere from the contralateral hemiretina appear to be weak or degraded. Stimuli could not be compared across the vertical meridian if the comparisons required detailed information on shape. Moreover, Fendrich and colleagues found no indication of overlap when stimuli were presented for only 200 ms. Only longer presentations indicated a dual representation of the retinal midline. The callosotomy research thus supports other work showing that macular sparing cannot be explained by nasotemporal overlap.
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Somatosensory processes are largely lateralized
The classic observations of the somatosensory system for a split-brain patient have not changed significantly. Following callosal section, stereognostic information processed by one hand is not available to the ipsilateral hemisphere (Gazzaniga et al., 1963
). Moreover, the presence or absence of light or deep touch can be detected by either hemisphere from both sides of the body, even though the ipsilateral stimulus is often ignored under conditions of bilateral stimulation.
More recent investigations have examined whether noxious stimuli can be represented bilaterally after unilateral stimulation (Stein et al., 1989). The conclusion was that, when noxious heat stimuli (43–47°C) were presented ipsilaterally to the responding hemisphere and were rated by the subject on a visual analogue scale, the ipsilateral hemisphere perceived the stimuli as far less intense than they actually were. The contralateral hemisphere perceived the stimulus intensity as in normal subjects, who rated it highly unpleasant. But when the stimuli reached the highest levels of heat intensity used in pain studies (49–51°C), the ipsilateral hemisphere perceived the stimulus intensity correctly (as does that of normal subjects) and the subjects rated the stimuli as highly unpleasant. Therefore, the emotional responses of the two hemispheres to the same stimulus are simultaneous but can be quite different. Thus, a variety of emotions evoked by at least some types of sensory stimuli are tightly coupled (sensory–affective coupling) to each hemisphere's perception of the attributes of the same sensory stimulus.
A disconnected hemisphere can control both arms but exerts only dominant control over the opposite hand
One of the enduring findings of split-brain research has been the distinction between a disconnected hemisphere's capacity for controlling proximal muscles versus distal muscles. Sectioning the callosum impairs the left hemisphere's ability to control the left hand and the right hemisphere's ability to control the right hand (Gazzaniga et al., 1967). These ipsilateral sensory-motor combinations need the intact callosum to integrate information from the cortical sensory areas to the motor cortex that controls distal hand movement. Either hemisphere can guide and control ipsilateral and contralateral movements involving the more proximal musculature of the shoulder, the upper arm, and of course the legs (Fig. 4).
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Prehension requires both the proximal musculature to transport the arm to the location of the desired object (i.e. reaching) and the distal musculature to adjust the shape of the hand to the intrinsic properties of the target (i.e. grasping) (Jeannerod, 1981
). Consequently, coordinating reaching and grasping may require that circuits lateralized to the ipsilateral and contralateral hemispheres interact. Johnson supports this hypothesis and goes on to say that this organization extends to motor planning as well as execution (Johnson, 1998; Johnson et al., 1999). Consistent with earlier work on motor control (e.g. Gazzaniga et al., 1967; Milner and Kolb, 1985), the left and right hemispheres have a knack for selecting the right way to grasp a target object with the contralateral hand. By contrast, only the left hemisphere evinces an advantage for choosing appropriate reaching movements. These results imply that the cerebral organization of motor planning is similar, but not identical, to those for motor control. In particular, the motor-dominant left hemisphere may be responsible for planning movements that include the proximal musculature of both arms. With the right arm, movements can be transferred via the corpus callosum to control mechanisms in the right hemisphere. Grasping, by contrast, can be planned and controlled only by the hemisphere contralateral to the relevant effector (Johnson et al., 1999). In the context of earlier motor control research, the apparent specialization of the left hemisphere for planning proximal movements reveals the pivotal role played by the corpus callosum in coordinating motor planning and control.
Support for the hypothesis that each hemisphere is specialized to represent movements of the contralateral hand is contained in a study of hand identification in callosotomy patients (Parsons et al., 1998). When asked to identify whether line drawings depict left or right hands—a task that involves imagining one's own hands in the position of the stimuli—each hemisphere displayed an advantage for identifying the contralateral versus the ipsilateral hand.
Split-brain patients can move their two arms in coordinated fashion
While the two arms can be individually governed by either hemisphere, it was uncertain whether bimanual coordination was possible. Split-brain patients can use their two hands in a seemingly coordinated fashion when performing tasks that require the integrated activity of the two hands. For example, patient J.W. is expert at the assembly of model cars, an activity that requires bilateral coordination. The production of actions requires planning at multiple levels in terms of the psychological processes and the underlying neural correlates of the processes. The central goal of current investigations has been to explore the extent of independence and interaction after callosotomy in components associated with the ability to carry out these coordinated movements.
There is decoupling of spatial but not temporal processes after callosotomy
Franz and colleagues (1996) showed that commissurotomized patients could coordinate two conflicting spatial programmes, whereas a normal control was impaired (Fig. 5). In effect, the spatial maps associated with a movement could be localized and isolated in each separated hemisphere. At the same time, while spatial information between the limbs remained separate, the temporal coordination of a bimanual movement remained largely intact.
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In following up a partially sectioned patient, Eliassen and colleagues discovered that the integration of direction information for two-handed movements takes place exclusively across the posterior corpus callosum (Eliassen et al., 1999
). They showed that the timing of a movement's initiation is affected by anterior and posterior callosotomy. The ability of the two hands to move simultaneously was affected by the callosal surgery. Thus, the distribution of spatial and temporal signals to integrate bimanual movement is dissociable with regard to callosal topography. Posterior cortical areas, the parietal lobes, are the source of a spatial motor signal used during bimanual movements. Eliassen and colleagues went on to show that anterior and posterior fibres are not equipotential (Eliassen et al., 2000). Anterior callosotomy disrupts the simultaneity of self-initiated bimanual movements more than it does the production of bimanual movements in response to a visual stimulus.
There is a subcortical locus for temporal coupling in bimanual movements after callosotomy
In studies by Tuller and Kelso and by Franz and colleagues, patient V.J. showed temporal coupling when asked to produce rhythmic bimanual movements (Tuller and Kelso, 1989; Franz et al., 1996). This observation has been replicated and extended by Ivry and colleagues (e.g. Ivry and Hazeltine, 1999). They discovered that the within-hand temporal variability of each hand was reduced (i.e. became more consistent) during bimanual tapping compared with unimanual tapping. This refutes neurological models that maintain that bimanual coupling arises from a common control signal isolated in one hemisphere. Rather, these results are consistent with the hypothesis that separable timing mechanisms are associated with each hand and are linked by a common subcortical signal for a response.
Either hemisphere can initiate saccadic eye movements
In contrast to the inability of a disconnected hemisphere to initiate ipsilateral hand movements with accuracy, each hemisphere can direct the eyes either contraversively or ipsiversively (Hughes et al., 1992). This capacity would not be predicted by dozens of studies showing that, in each hemisphere, the frontal eye fields control only contraversive eye movements (Wurtz and Albano, 1980; Bruce and Goldberg, 1984). What is more, preliminary evidence (Fendrich et al., 1998) shows that, despite the absence of a corpus callosum, either hemisphere can monitor the amplitude of saccades initiated by the other hemisphere even when no visual feedback is available. This finding is noteworthy because it is generally thought that saccades are primarily monitored via a `corollary discharge' derived from the motor commands sent to the eye muscles. In this instance, regardless of which hemisphere issues the commands, the corollary discharge is routed to both hemispheres from a subcortical locus. Fendrich and colleagues similarly found that each hemisphere can initiate both an ipsiversive and a contraversive oculomotor pursuit (Fendrich et al., 1990). Such results reveal how psychophysical studies of patients with discrete lesions can illuminate neural pathways that might otherwise not be evident.
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Attentional, perceptual and cognitive interaction after hemisphere disconnection |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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The attentional and perceptual abilities of split-brain patients have been explored extensively. It now appears that function is duplicated between the hemispheres in basic perceptual processes; this may proceed independently in the two hemispheres, even in the absence of the corpus callosum. However, the situation is more complicated for attentional processes, where some forms of attention are integrated at the subcortical level and other forms act independently in the separated hemispheres. In contrast, higher-level cognitive and linguistic processes involve hemispheric specialization, so callosal pathways are necessary to integrate these functions.
Simple perceptual interactions are not seen
Split-brain patients cannot cross-integrate visual information between their two half visual fields. When visual information is lateralized to either the left or the right disconnected hemisphere, the unstimulated hemisphere cannot use the information for perceptual analysis. This is also true for stereognostic information presented to each hand. While the presence or absence of touch stimulation is noted in any part of the body by either hemisphere, patterned somatosensory information is lateralized. Thus, an object held in the left hand cannot help the right hand find an identical object. Although some have argued that certain higher-order perceptual information is integrated at some level by way of subcortical structures (Cronin-Golomb, 1986; Sergent, 1990), these results have not been replicated by others (McKeever et al., 1981; Corballis et al., 1993; Corballis, 1994; Seymour et al., 1994; Funnell et al., 1999).
Subcortical transfer of higher-order information is more apparent than real
Kingstone and Gazzaniga found that split-brain patients will sometimes draw a picture that combines word information presented separately to the two hemispheres. for example, from a left visual field (LVF) stimulus of `ten' and a right visual field (RVF) stimulus of `clock', the subject draws a picture of a clock set at 10 o'clock (Kingstone and Gazzaniga, 1995). Although this outcome initially seemed to imply the subcortical transfer of higher-order information between the hemispheres, subsequent observations revealed that it reflects dual-hemisphere control of the drawing hand (biased to the left hemisphere). Conceptually ambiguous word pairs, such as `hot' + `dog', were always depicted literally (e.g. a dog panting in the heat) and never as emergent objects (e.g. a frankfurter; Fig. 15). Moreover, right- and left-hand drawings often depicted only the words presented to the left hemisphere.
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Interhemispheric transfer is seen for crude spatial location information
Unlike visual and somatosensory cues, crude information concerning spatial locations can be cross-integrated (Trevarthen, 1968
; Trevarthen and Sperry, 1973; Holtzman, 1984). In one experiment, a four-point grid was presented to each visual field (Fig. 6A). On a given trial, one of the positions on the grid was highlighted and one condition of the task required the subject to move his eyes to the highlighted point within the visual field stimulated. In the second condition, the subject was required to move his eyes to the relevant point in the opposite visual field. Split-brain subjects could do this at above-chance levels, perhaps because of crude cross-integration of spatial information. This was true even if the grid was positioned randomly in the tested field.
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Spatial attention can be directed but not divided between the hemispheres
The finding that some type of spatial information remains integrated between the two half-brains raises a question: are the attentional processes associated with spatial information affected by cortical disconnection surgery? Using a modification of a paradigm developed by Posner and colleagues (Posner et al., 1980
) that capitalizes on priming phenomena, Holtzman and colleagues (Holtzman et al., 1981) found that either hemisphere can direct attention to a point in either the left or right visual field (Fig. 6B
). Posner first showed that the response latency to a peripheral visual target is reduced when observers have prior information regarding its spatial locus, even when eye movements are prevented. The spatial cue presumably allows observers to direct their attention to the location prior to the onset of the target. When this paradigm was used in split-brain patients to measure how much attentional cues affect performance, the separated hemispheres were not strictly independent in their control of spatial orientation. Rather, the two hemispheres relied on a common orienting system to maintain a single focus of attention. Thus, as with normal people, a cue to direct attention to a point in the visual field is used no matter which hemisphere gets the cue.
The discovery that spatial attention can be directed with ease to either visual field raised another question: can each separate cognitive system in the split-brain patient independently direct attention to a part of its own visual field (Holtzman et al., 1984)? Can the right hemisphere direct attention to a point in the left visual field while the left brain simultaneously attends to a point in the right visual field? Normal subjects cannot so divide their attention. Can split-brain patients do so?
The split-brain patient cannot divide spatial attention between the two half-brains (Reuter-Lorenz and Fendrich, 1990). There appears to be only one integrated spatial attention system that remains intact after cortical disconnection (Fig. 6B). This is consistent with electrophysiological studies showing that event-related potentials associated with simultaneous target detections in the two visual fields are not elicited independently in the separated hemispheres (Kutas et al., 1990). Thus, like neurologically intact observers, the attentional system of split-brain patients is unifocal. They cannot prepare for events in two spatially disparate locations.
Attentional resources are shared
Even though there seems to be but one focus of attention, the dramatic effects of disconnecting the cerebral hemispheres on perception and cognition might suggest that each half-brain possesses its own attentional resources. If this were true, one would predict that the cognitive operations of one half-brain, no matter what the difficulty, would have only a slight influence on the other's cognitive activities. The competing view is that the brain has limited resources for managing such processes; if resources are being applied to task A, fewer are available for task B. This model maintains that the harder one hemisphere works on a task, the worse the other hemisphere does on a task of constant complexity.
Many investigations have focused on this issue; all confirm the notion that the central resources are limited (Holtzman and Gazzaniga, 1982; Reuter-Lorenz et al., 1996). In the original experiment, two series of geometrical shapes were displayed concurrently to the left and right of central fixation and hence were lateralized to the right and left hemispheres (Fig. 7). A unilateral probe figure appeared subsequently, and the observer indicated with a forced-choice key press whether it matched any of the field's items. In half of the trials the same three figures were displayed in the two fields—the hard condition. In the other half, one hemisphere saw three items while the other saw only one stimulus presented three times, the latter being the easy condition. The results proved that when one half-brain was working on processing only one repeated stimulus, the opposite hemisphere was better at recalling whether the probed stimulus was part of the original three stimuli. When both hemispheres were trying to process three stimuli, the performance of each hemisphere was impaired. These findings have been replicated in a monkey model of the tasks (Lewine et al., 1994).
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Other experiments address attentional sharing (Pashler et al., 1994
; Ivry et al., 1998). Split-brain patients have a psychological refractory period effect between the two hemispheres, an indication that tasks being presented to each half-brain alone are being correlated. When one hemisphere discriminates a stimulus and makes a choice, this delays the other hemisphere in making a similar choice. At the same time, the patients fail to exhibit attentional costs between the hemispheres. For example, split-brain patients do not show the cost that normal subjects reveal when they use two hands for the two responses: they maintain incompatible response codes for each hand.
Division of cognitive resources can improve performance
In the callosum-sectioned patient, no measurable interactions happen between the two hemispheres during the processing of perceptual information. Identical and simple visual patterns of all kinds can be presented to each separate half-brain and the patient cannot say whether the stimuli are the same or different. This raises the possibility that, in a memory test of visual retention, a split-brain subject might perform at a higher level than a normal subject if the perceptual information were distributed between the two visual half fields. For example, a complex spatial memory task was administered to a split-brain patient and normal controls; critical information was presented in each visual half-field (Holtzman and Gazzaniga, 1985). For normal subjects, the visual information was automatically combined and perceived as one large problem. For the split-brain patient, each hemisphere perceived a problem that remained separate from the perceptual information presented to the other half-brain; thus, each hemisphere perceived a much simpler task. The results were clear: the split-brain patient outperformed the normal subjects. The callosum-sectioned patient benefited from the fact that the perceptual array under one of the test conditions did not seem to be more difficult because the work was distributed to each separate hemisphere, even though the sensory array was identical to that experienced by the normal subjects.
There is no question that disconnection of the cerebral hemispheres allows a unique cognitive state. In a sense it turns a unified perceptual system into two simpler perceptual systems that do not interact and therefore do not interfere with each other. It allows the breaking down of a large perceptual problem into smaller, more manageable problems that a half-brain can solve. From the observer's point of view, though, it looks as if the patient's total information processing capacity has increased and is superior to that of normal subjects. Yet, as we noted for attention, split-brain patients do not have more resources to call on to solve problems. The human brain has a set number of resources it can allocate to cognitive tasks, and these resources remain constant after commissurotomy. How, then, do we explain these two different results? Performance seems better than normal yet perceptual and cognitive tasks have limited resources.
The conundrum forces the issues of where in a perceptual–motor task the resources are applied. Are they, for example, applied during the early phases of information processing, which deal with the complexity of the visual stimulus itself? Or are the resources applied at later loci of the information processing sequence to handle more cognitive aspects? Interactions between the hemispheres on resource limits may occur when the task is more cognitive and requires a working memory. Lewine and colleagues have proposed a similar scheme and suggest that the site of subcortical interaction may be the brainstem (Lewine et al., 1994).
Visual search may proceed independently in separated half-brains
While the resources a brain commits to a task appear constant, their method of deployment can vary. The more items to be analysed in a visual array, the longer it takes. After a baseline reaction time has been established it takes normal controls an additional 70 ms to respond to two more items, another 70 ms for an additional two items, and so on. In split-brain patients, when the items are distributed across the midline of the visual field, as opposed to being in one visual field, the reaction time to added stimuli is cut in half (Fig. 8) (Luck et al., 1989, 1994).
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This notion was extended by Kingstone and colleagues when they discovered that the strategy differs according to which hemisphere examines the contents of its visual field (Kingstone et al., 1995
). The left-dominant hemisphere uses a `guided' or `smart' strategy whereas the right hemisphere does not. This means that the left hemisphere adopts a helpful cognitive strategy in solving the problem whereas the right hemisphere does not possess those extra cognitive skills. But it does not mean that the left hemisphere is always superior to the right hemisphere in attentional orienting.
Kingstone and colleagues have demonstrated that the right hemisphere, which is superior to the left hemisphere for processing upright faces, shifts attention automatically to where someone is looking (Kingstone et al., 2000). The left hemisphere does not demonstrate a similar attentional response to gaze direction.
The act of independent scanning in the hemispheres of split-brain patients during visual search appears contrary to the sharing of attentional resources. At this time, this issue remains unresolved and more research is needed. However, it should be mentioned that this apparent discrepancy may reflect the fact that multiple mechanisms of attention appear to operate at different stages of processing, some of which might be shared across the disconnected hemispheres and others of which might be independent (Luck and Hillyard, 2000). Luck and Hillyard describe evidence that the psychological refractory period paradigm reflects a late attentional mechanism, whereas visual search reflects an early attentional mechanism.
Attentional orienting differs qualitatively between the hemispheres
Kingstone and colleagues have noted that the hemispheres interact quite differently in their control of reflexive (exogenous) and voluntary (endogenous) attentional processes (Enns and Kingstone, 1997; Kingstone et al., 1997, 2000). The evidence suggests that reflexive attentional orienting happens independently in the two hemispheres, while voluntary attentional orienting involves hemispheric competition with control preferentially lateralized to the left hemisphere. These data explain not only the low-level sensory effects of attentional orienting but also bear on more complex behaviours, such as visual search. For instance, when the number of items to be searched is small, attentional orienting is largely reflexive in nature, and the two hemispheres perform independently (Luck et al., 1989, 1994). But when the number of items to be searched is large, or the search is strategic, attentional orienting is largely volitional and attentional orienting is lateralized to the left hemisphere (Kingstone et al., 1995). Mangun and colleagues have also shown that the right hemisphere has a predominant role in attentional orienting (Mangun et al., 1994). Indeed, even in callosally sectioned patients, the right hemisphere attends to the entire visual field whereas the left hemisphere attends only to the right field. This finding has also been noted by Berlucchi and colleagues (Berlucchi et al., 1997) and by Corballis (Corballis, 1995).
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Perceptual asymmetries following cerebral disconnection |
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TopAbstractIntroductionGeneral backgroundPatient populationBasic neurological mechanismsAttentional, perceptual and...Perceptual asymmetries following...Partial callosal section reveals...Memory studies after cerebral...Language and speech processes...Studies related to issues...Implications for understanding...References |
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Hemispheric asymmetries in visuospatial processing have long been observed (e.g. Gazzaniga et al., 1967). Nevertheless, the fundamental nature of these asymmetries and how they arose remain unclear. Initial studies with split-brain patients found that the right hemisphere outperformed the left at a variety of visuospatial tasks such as block design and drawing three-dimensional objects (Bogen and Gazzaniga, 1965
; Gazzaniga et al., 1965). These findings contributed to the popular notion that the right hemisphere is specialized for visuospatial processing. Subsequently, a number of researchers proposed dichotomies suggesting that the two hemispheres process information in different, though complementary, ways. For example, Sergent suggested that the left hemisphere selectively processes the high-spatial-frequency information in a stimulus and the right hemisphere selectively processes the low-spatial-frequency information (Sergent, 1982). Similarly, Lamb and colleagues proposed that the left hemisphere processes the local details of a stimulus, whereas the right hemisphere processes its global layout (Lamb et al., 1989). Finally, Kosslyn and colleagues proposed that the left hemisphere tends to represent visuospatial information `categorically' (representing the relations between stimuli descriptively: above, below, left, right) (Kosslyn et al., 1989). The right hemisphere, by contrast, was posited to represent visuospatial information in a finer-grained, `coordinate' framework.
Each of these dichotomies suggests that the hemispheres both contribute their expertise to the overall processing of the stimulus, effectively dividing the workload between them. While these theories have each received some empirical support, there has been relatively little effort to test them directly in the split brain. Fendrich and Gazzaniga, though, did examine the Sergent hypothesis concerning hemispheric differences in sensitivity to differing spatial frequencies (Fendrich and Gazzaniga, 1989). In this study, split-brain patients compared the orientations of two grating patches presented briefly within a single visual hemifield. Performance declined with increasing spatial frequency in both visual fields. The data failed to support the hypothesis that the right hemisphere is specialized for processing low spatial frequencies and the left for high spatial frequencies.
An alternative view is that perceptual asymmetries do not necessarily reflect a division of labour between the hemispheres, but are a consequence of other, more primitive, hemispheric specializations (Gazzaniga, 1970, 1998; Corballis et al., 2000). As left-hemisphere specialization for linguistic (and temporal) processing evolved, cortical tissue that had been dedicated to visuospatial processing was co-opted, resulting in the loss of visuospatial abilities in the left hemisphere (Fig. 9). This cost is illustrated in a series of experiments we have conducted recently.
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There is right-hemisphere superiority for perceptual grouping processes
In order to perceive objects in the environment as unified wholes, the visual system must often extrapolate from incomplete information about contours and boundaries. For example, there are conditions in which object contours are perceived in areas of completely homogeneous stimulation. Because these object boundaries are not present in the physical stimulus, they are referred to as `illusory contours'. Illusory contours are often perceived when the edges of elements in the visual array are consistent with the presence of a superimposed surface or object, despite the lack of a brightness transition to signal an object contour (Kanizsa, 1976
, 1979). Similarly, the shape of an object can often be perceived correctly in spite of the fact that some other object or surface occludes a significant proportion of its contour. The process underlying the perception of the shape in this case is termed `amodal completion' (Michotte, 1964; Kanizsa, 1979).
Several authors have suggested that the same mechanism is responsible for both illusory contour perception and amodal completion (Kellman and Loukides, 1987; Kellman and Shipley, 1991; Ringach and Shapley, 1996). Furthermore, there is some evidence that this mechanism is preferentially lateralized to the right cerebral hemisphere. Illusory contours and amodal completion are often cited as examples of the Gestalt `closure' principle, which refers to the experience of a bounded perceptual unit from partial or disorganized information (e.g. Koffka, 1924). Several studies have suggested that the right hemisphere plays a critical role in perceptual closure processes (e.g. De Renzi and Spinnler, 1966; Wasserstein et al., 1987; Hirsch et al., 1995).
Corballis and colleagues investigated boundary completion by illusory contours and amodal completion in split-brain subjects (Corballis et al., 1999). These processes were assessed using a lateralized shape discrimination task similar to that employed by Ringach and Shapley (Ringach and Shapley, 1996). In this task the subject is required to judge whether a deformed Kanizsa rectangle appears `thin' or `fat' (Fig. 10). Performance is compared with that in a control task in which the pacmen all face in the same direction and the participant is required to judge whether they are tilted `up' or `down'. Ringach and Shapley showed that neurologically intact observers are significantly better at the shape discrimination task than the control task, which indicates that the boundary-completion process assists in making the discrimination. The difference in performance between the two conditions provides an index of the perceptual strength of the boundary completion.
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The first experiment (Corballis et al., 1999
) investigated the generation of illusory contours by the isolated hemispheres of two right-handed callosotomy patients, J.W. and V.P. Patient J.W.'s performance for both left-hemifield and right-hemifield stimuli was significantly improved by the presence of illusory contours. This indicates that J.W.'s two hemispheres are equally capable of generating illusory contours. Patient V.P. also showed improved discrimination accuracy when illusory contours were present, although this was restricted to stimuli presented to the right hemifield. This indicates that V.P.'s left hemisphere, at least, is capable of generating illusory contours. Her discrimination performance for left-hemifield stimuli was good, so it seems likely that the lack of an advantage for illusory contour stimuli was the result of a ceiling effect. Overall, the results of this experiment suggest that, although the right hemisphere is better at the angular discrimination task, the two hemispheres profit equally from the presence of illusory contours.
Corballis and colleagues also compared the generation of illusory contours with amodal boundary completion in each hemisphere of patients J.W. and V.P. (Corballis et al., 1999). If both tasks were mediated by the same neural mechanism there should be no systematic differences in performance between the two hemispheres. Both patients showed marked asymmetry in performance when discrimination depended on amodal completion. Amodal completion was performed well by the right hemisphere, but was poor in the left hemisphere. This finding strongly suggests that some aspect of the mechanism supporting amodal completion is lateralized to the right hemisphere. Taken together, these data suggest that several dissociable mechanisms contribute to boundary completion, and that these mechanisms are lateralized differently.
An intriguing aspect of this finding is that mice can apparently perceive shapes by amodal completion (Kanizsa et al., 1993), which suggests that the grouping process that is lateralized to the right hemisphere is not a recent evolutionary adaptation. This has led to the current speculation that the right-hemisphere `specialization' for visuospatial processing may be the result of the left hemisphere losing the visuospatial abilities it once possessed.
There is a left-hemisphere matching deficit for visual stimuli
Recently, we have been studying the hypothesis that the left hemisphere is capable of sophisticated visual processing but represents spatial information relatively crudely compared with the right hemisphere (Corballis et al., 1999; Funnell et al., 1999). The implication of this hypothesis is that pattern recognition is a function of both hemispheres but the right hemisphere is further specialized for processing spatial information. Several recent results support this hypothesis. First, Funnell and colleagues discovered that the left hemisphere of split-brain patient J.W. was impaired relative to the right hemisphere in deciding whether two visually presented objects were identical or mirror-reversed (Funnell et al., 1999). This deficit was similar in magnitude for a variety of stimulus manipulations. In a follow-up study, Corballis and colleagues (unpublished results) found similar left-hemisphere deficits in patients J.W. and V.P. for judgements requiring spatial discriminations (size, orientation and vernier acuity) but not for those requiring non-spatial discrimination (luminance).
Corballis and colleagues conducted a more explicit test of the hypothesis that the major difference in visual function between the hemispheres is a right-hemisphere specialization for representing spatial relationships (Corballis et al., 1999). They presented patients J.W. and V.P. with pairs of stimuli within a single visual hemifield. These stimuli consisted of a square frame that contained a small icon in one corner. In one condition (the `identity