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Brain (2000), 123, 1293–
I N V I T E D R E V I E W
Cerebral specialization and interhemispheric
communication
Does the corpus callosum enable the human condition?
Michael S. Gazzaniga
Center for Cognitive Neuroscience, Dartmouth College, Correspondence to: Michael S. Gazzaniga, Center for Hanover, New Hampshire, USA Cognitive Neuroscience, Dartmouth College, Hanover, NH 03755, USA
Summary
The surgical disconnection of the cerebral hemispheres half-brain. By having the callosum serve as the great creates an extraordinary opportunity to study basic communication link between redundant systems, a pre- neurological mechanisms: the organization of the sensory existing^ system^ could^ be^ jettisoned^ as^ new^ functions and motors systems, the cortical representation of the developed in one hemisphere, while the other hemisphere perceptual and cognitive processes, the lateralization of could continue to perform the previous functions for both function, and, perhaps most importantly, how the divided half-brains. Split-brain studies have also revealed the brain yields clues to the nature of conscious experience. complex mosaic of mental processes that participate in Studies of split-brain patients over the last 40 years human cognition. And yet, even though each cerebral have resulted in numerous insights into the processes of hemisphere has its own set of capacities, with the left perception, attention, memory, language and reasoning hemisphere^ specialized^ for^ language^ and^ speech^ and abilities. When the constellation of findings is considered major^ problem-solving^ capacities^ and^ the^ right hemisphere specialized for tasks such as facial recognition as a whole, one sees the cortical arena as a patchwork of and attentional monitoring, we all have the subjective specialized processes. When this is considered in the light (^) experience of feeling totally integrated. Indeed, even of new studies on the lateralization of functions, it becomes (^) though many of these functions have an automatic quality reasonable to suppose that the corpus callosum has (^) to them and are carried out by the brain prior to our enabled the development of the many specialized systems (^) conscious awareness of them, our subjective belief and by allowing the reworking of existing cortical areas (^) feeling is that we are in charge of our actions. These while preserving existing functions. Thus, while language (^) phenomena appear to be related to our left hemisphere’s emerged in the left hemisphere at the cost of pre-existing (^) interpreter, a device that allows us to construct theories perceptual systems, the critical features of the bilaterally about the relationship between perceived events, actions present perceptual system were spared in the opposite and feelings.
Keywords : cerebral specialization; callosum; interhemispheric; interpreter
Abbreviations : HERA hemispheric encoding/retrieval asymmetry; LVF left visual field; RVF right visual field; SOA stimulus-onset asynchrony
Introduction
In the pages of this journal much of the original work on the intellectual basis for a new behavioural neurology, disconnection syndromes has been described, especially the particularly in the USA. In what follows I review progress effects of surgical section on the corpus callosum. Over 30 in studying patients with surgical disconnection of the cerebral years ago, Norman Geschwind’s magnificent two-part review hemispheres. I concentrate on research over the past 40 years, article on disconnection syndromes (Geschwind, 1965 a , b ) especially as it relates to current views of the human brain’s launched not only a thousand research ships but provided neurological organization. This work is of a particular kind
© Oxford University Press 2000
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in that each cerebral hemisphere is examined with the functions and that the right hemisphere has even more help of specialized stimulus lateralization techniques. These (^) prominent limitations in its cognitive functions. The model techniques have evolved over years of testing and they (^) thus maintains that lateral specialization reflects the allow unique ways of interpreting the neuropsychological (^) emergence of new skills and the retention of others. Natural assessment of these surgical cases. As a consequence, studies (^) selection allowed this odd state of affairs because the callosum that do not use these testing procedures are limited and will (^) integrated these developments in a functional system that not be reviewed. (^) 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
General background appears that the developing child and the rhesus monkey
The human brain is a bizarre device, set in place through (^) have similar cognitive abilities (Hauser and Carey, 1998). It natural selection for one main purpose—to make decisions (^) has been shown that many simple mental capacities, such as that enhance reproductive success. That simple fact has many (^) classification tasks, are possible in the monkey and in the consequences and is at the heart of evolutionary biology. (^) 12-month-old child. Yet many of these capacities are not Once grasped, it helps the brain scientist to understand a (^) evident in the right hemisphere of a split-brain subject major phenomenon of human brain function—its ubiquitous (^) (Funnell and Gazzaniga, 2000). It is as if the right lateral cerebral specialization. Nowhere in the animal (^) hemisphere’s attention–perception system has co-opted these kingdom is there such rampant specialization of function. (^) capacities, just as the emerging language systems in the left Why is this, and how did it come about? (^) hemisphere co-opt its capacity for perception. What emerges from split-brain research is a possible insight (^) With these changes ongoing, one might predict that there to these questions. It may turn out that the oft-ignored corpus (^) would be an increase in local intrahemispheric circuitry and callosum, a fibre tract that is thought merely to exchange (^) a reduced interhemispheric circuitry. With local circuits information between the two hemispheres, was the great (^) becoming specialized and optimized for particular functions, enabler for establishing the human condition. Non-human (^) the formerly bilateral brain need no longer keep identical brains, by contrast, reveal scant evidence for lateral (^) processing systems tied together for all aspects of information specialization, except as rarely noted, for example, by (^) processing. The communication that occurs between the two Hamilton and Vermeire while they were investigating the hemispheres can be reduced, as only the products of the macaque monkey’s ability to perceive faces (Hamilton and processing centres need be communicated to the opposite Vermeire, 1988). In that study, they discovered a right half-brain. Recently, Rilling and Insel have reported that hemisphere superiority for the detection of monkey faces. there is a differential expansion of cerebral white matter With the growing demand for cortical space, perhaps the relative to the corpus callosum in primates (Rilling and Insel, forces of natural selection began to modify one hemisphere 1999). Humans show a marked decrease in the rate of growth but not the other. Since the callosum exchanges information between the two hemispheres, mutational events could occur of^ the^ corpus^ callosum^ compared^ with^ intrahemispheric in one lateralized cortical area and leave the other mutation- comparisons of white matter. free, thus continuing to provide the cortical function from There is also new evidence that could lead the way to the homologous area to the entire cognitive system. As discovering how new functions, exclusively human in nature, these new functions develop, cortical regions that had been arise during cortical evolution. Neurons in the monkey’s dedicated to other functions are likely to be co-opted. Because prefrontal lobe respond not only when the animal is going these functions are still supported by the other hemisphere, to grasp a piece of food but also when the human experimenter there is no overall loss of function. In short, the callosum is about to grasp the same piece of food (Rizzolatti^ et al ., allowed a no-cost extension; cortical capacity could expand 1996). It would appear that circuits in the monkey brain by reducing redundancy and extending its space for new make it possible for the monkey to represent the actions of cortical zones. others. Rizzolatti (Rizzolatti, 1998) suggested that such a This proposal is offered against a backdrop of new findings system might be the seed for the uniquely human theory of in cognitive neuroscience, findings that strongly suggest a mind module (Baron-Cohen, 1995). how important local, short connections are for the proper It is against this backdrop—one in which developmental maintenance and functioning of neural circuits (Cherniak, and evolutionary time come into play and a dynamic cortical 1994; Allman, 1999). Long fibre systems are relevant—most system^ establishes^ adaptations^ that^ become^ laterally likely for communicating the products of a computation— specialized systems—that I review research on hemispheric but short fibres are crucial for producing the computation in^ disconnection syndromes. First, I examine basic neurological question. Does this mean that as the computational needs for systems related to the senses, and then I consider issues in specialization increase there is pressure to sustain mutations motor control. The evolutionary perspective creeps in early that alter circuits close to a nascent site of activity? as we see similarities and differences in organization between One of the major facts emerging from split-brain research the monkey and human visual systems. Building on these is that the left hemisphere has marked limitations in perceptual aspects, I survey perceptual and cognitive issues that have
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Fig. 1 To examine hemispheric processing differences differentially it is necessary to lateralize stimuli within the left and right visual fields. In early studies this was managed with a mechanically driven tachistoscope, as depicted in A. Tactile stimuli were also presented out of view to either hand. More recently, lateralized computer presentations have replaced the tachistoscope (shown in B ). As shown in the centre panel, however, proper lateralization is not achieved if the subject makes an eye movement during the stimulus presentation ( upper middle ). The development of retinal stabilization procedures makes it possible now to counteract the effects of such eye movements. The Purkinje eye-tracking and image-stabilizing device is depicted in the right panel of B. Coupled with a mirror stimulus deflector, this dual Purkinje image eyetracker allows retinal stabilization. As eye movements occur, horizontal and vertical deflection mirrors move to counteract these movements, maintaining proper lateralization.
crowded out by the addition of specialized regions that Whether the anatomical projections have any functional developed in the anterior regions of the visual system. This significance has never been established, but there has been left the anterior commissure for olfactory and non-visual speculation that this zone might be responsible for the communication. Regions involved in early stages of visual phenomenon of ‘macular sparing’ (Bunt and Minkler, 1977; processing would remain unaffected by the addition of these Leventhal et al ., 1988). Strokes affecting the primary visual new functional regions. This is consistent with the view that cortex in either hemisphere produce blindness in the opposing there are no major interspecies differences in the early stages visual field, but within the blind field a small region of central of the visual system. 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,
Humans have visual midline overlap in neurologically normal subjects, attempts to demonstrate
phenomena this zone psychophysically have failed consistently (e.g.
Nasotemporal overlap at the retinal vertical meridian in cat Harvey, 1978; Lines and Milner, 1983). Fendrich and and monkey is readily evident (Stone, 1966; Stone et al ., colleagues have examined this in split-brain subjects 1973; Bunt and Minkler, 1977; Leventhal et al ., 1988). In a (Fendrich and Gazzaniga, 1989; Fendrich et al. , 1994). Using 1 – 2 ° stripe that straddles the two visual half-fields, visual an image stabilizer in combination with a Purkinje eyetracker, information is sent to the left and right visual cortices. careful assessment of the visual midline of two split-brain
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Fig. 2 Only the corpus callosum is sectioned in most split-brain operations performed on humans. In the split-brain patients who underwent surgery in California, however, the anterior (^) Fig. 3 The clinical phenomenon of macular sparing by commissure was also sectioned. Behavioural testing on patients (^) nasotemporal overlap has been explained traditionally by with and without sparing of the anterior commissure reveals no hypothesizing a zone of overlap that encompasses the entire evidence for visual transfer of information in any of these fovea. In contrast, data from callosotomy patients suggest that the patients. The anterior commissure, therefore, does not appear to zone does not encompass the entire fovea but rather remains support any functional transfer in humans. In split-brain monkeys, narrow as it crosses the fovea. There is additional evidence that it however, leaving the anterior commissure intact does allow the may be wider in the upper hemiretina (lower visual field) than in interhemispheric transfer of visual information, even when the the lower hemiretina. body of the corpus callosum is sectioned.
patients has revealed an area no more than 2° wide at the hand is not available to the ipsilateral hemisphere (Gazzaniga veridical midline where some visual information appears et al ., 1963). Moreover, the presence or absence of light or available to each half-brain (Fig. 3). This contrasts with the deep touch can be detected by either hemisphere from both findings of Sugishita and colleagues, who found no evidence sides of the body, even though the ipsilateral stimulus is of overlap in hemianopic subjects but did not have the often ignored under conditions of bilateral stimulation. advantage of image stabilization and were restricted to only More recent investigations have examined whether noxious brief stimulus presentations (Sugushita et al. , 1994). The stimuli can be represented bilaterally after unilateral strip of overlap does not encompass the entire fovea. Within stimulation (Stein et al ., 1989). The conclusion was that, when this strip the signals conveyed to each hemisphere from the noxious heat stimuli (43– 47 °C) were presented ipsilaterally to contralateral hemiretina appear to be weak or degraded. the responding hemisphere and were rated by the subject on Stimuli could not be compared across the vertical meridian a visual analogue scale, the ipsilateral hemisphere perceived if the comparisons required detailed information on shape. the stimuli as far less intense than they actually were. The Moreover, Fendrich and colleagues found no indication of contralateral hemisphere perceived the stimulus intensity as overlap when stimuli were presented for only 200 ms. Only in normal subjects, who rated it highly unpleasant. But when longer presentations indicated a dual representation of the the stimuli reached the highest levels of heat intensity retinal midline. The callosotomy research thus supports other used in pain studies (49– 51 °C), the ipsilateral hemisphere work showing that macular sparing cannot be explained by perceived the stimulus intensity correctly (as does that of nasotemporal overlap. 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
Somatosensory processes are largely lateralized be quite different. Thus, a variety of emotions evoked by at
The classic observations of the somatosensory system for a least some types of sensory stimuli are tightly coupled split-brain patient have not changed significantly. Following (sensory–affective coupling) to each hemisphere’s perception callosal section, stereognostic information processed by one of the attributes of the same sensory stimulus.
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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
Fig. 5 The disconnection between the spatial maps of the two of which hemisphere issues the commands, the corollary hemispheres in split-brain patients is illustrated in this paradigm. discharge is routed to both hemispheres from a subcortical Subjects are shown two figures, one in each visual field, and locus. Fendrich and colleagues similarly found that each asked to draw the stimuli with both hands simultaneously. (^) hemisphere can initiate both an ipsiversive and a contraversive Neurologically normal subjects are able to perform this bimanual (^) oculomotor pursuit (Fendrich et al ., 1990). Such results task when the two stimuli are identical or mirror-reversed but not when the stimuli result in incompatible spatial maps. Split-brain reveal how psychophysical studies of patients with discrete patients, however, show no deficit in this latter condition and their lesions can illuminate neural pathways that might otherwise performance is strikingly better than that of normal subjects. The not be evident. split-brain patient is able to carry out conflicting motor programmes, indicating that the spatial representations of movements are clearly maintained and isolated to each
hemisphere (adapted from Franz et al ., 1996). Attentional, perceptual and cognitive
interaction after hemisphere disconnection
anterior and posterior fibres are not equipotential (Eliassen (^) The attentional and perceptual abilities of split-brain patients et al ., 2000). Anterior callosotomy disrupts the simultaneity (^) have been explored extensively. It now appears that function of self-initiated bimanual movements more than it does the (^) is duplicated between the hemispheres in basic perceptual production of bimanual movements in response to a visual (^) processes; this may proceed independently in the two stimulus. (^) 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
There is a subcortical locus for temporal the subcortical level and other forms act independently in
coupling in bimanual movements after the separated hemispheres. In contrast, higher-level cognitive
callosotomy and linguistic processes involve hemispheric specialization,
In studies by Tuller and Kelso and by Franz and colleagues, so callosal pathways are necessary to integrate these functions. 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 Simple perceptual interactions are not seen
extended by Ivry and colleagues (e.g. Ivry and Hazeltine, Split-brain patients cannot cross-integrate visual information 1999). They discovered that the within-hand temporal between their two half visual fields. When visual information variability of each hand was reduced (i.e. became more is lateralized to either the left or the right disconnected consistent) during bimanual tapping compared with hemisphere, the unstimulated hemisphere cannot use the unimanual tapping. This refutes neurological models that information for perceptual analysis. This is also true for maintain that bimanual coupling arises from a common stereognostic information presented to each hand. While the control signal isolated in one hemisphere. Rather, these presence or absence of touch stimulation is noted in any part
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of the body by either hemisphere, patterned somatosensory phenomena, Holtzman and colleagues (Holtzman et al. , 1981) information is lateralized. Thus, an object held in the left found that either hemisphere can direct attention to a point hand cannot help the right hand find an identical object. in either the left or right visual field (Fig. 6B). Posner first Although some have argued that certain higher-order showed that the response latency to a peripheral visual target perceptual information is integrated at some level by way of is reduced when observers have prior information regarding subcortical structures (Cronin-Golomb, 1986; Sergent, 1990), its spatial locus, even when eye movements are prevented. these results have not been replicated by others (McKeever The spatial cue presumably allows observers to direct their et al ., 1981; Corballis et al ., 1993; Corballis, 1994; Seymour attention to the location prior to the onset of the target. When et al ., 1994; Funnell et al ., 1999). 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
Subcortical transfer of higher-order information spatial orientation. Rather, the two hemispheres relied on a
is more apparent than real common orienting system to maintain a single focus of
Kingstone and Gazzaniga found that split-brain patients will attention. Thus, as with normal people, a cue to direct sometimes draw a picture that combines word information attention to a point in the visual^ field is used no matter which presented separately to the two hemispheres. for example, hemisphere gets the cue. from a left visual field (LVF) stimulus of ‘ten’ and a right The discovery that spatial attention can be directed with visual field (RVF) stimulus of ‘clock’, the subject draws a ease^ to^ either^ visual^ field^ raised^ another^ question:^ can picture of a clock set at 10 o’clock (Kingstone and Gazzaniga, each separate cognitive system in the split-brain patient 1995). Although this outcome initially seemed to imply the independently direct attention to a part of its own visual^ field subcortical transfer of higher-order information between the (Holtzman^ et al ., 1984)? Can the right hemisphere direct hemispheres, subsequent observations revealed that it reflects attention to a point in the left visual^ field while the left brain dual-hemisphere control of the drawing hand (biased to the simultaneously attends to a point in the right visual^ field? left hemisphere). Conceptually ambiguous word pairs, such Normal subjects cannot so divide their attention. Can split- as ‘hot’ ‘dog’, were always depicted literally (e.g. a dog brain patients do so? panting in the heat) and never as emergent objects (e.g. a The^ split-brain^ patient^ cannot^ divide^ spatial^ attention frankfurter; Fig. 15). Moreover, right- and left-hand drawings between the two half-brains (Reuter-Lorenz and Fendrich, often depicted only the words presented to the left hemisphere. 1990).^ There^ appears^ to^ be^ only^ one^ integrated^ spatial attention system that remains intact after cortical disconnec- tion (Fig. 6B). This is consistent with electrophysiological studies showing that event-related potentials associated with
Interhemispheric transfer is seen for crude
simultaneous target detections in the two visual fields are
spatial location information not elicited independently in the separated hemispheres
Unlike visual and somatosensory cues, crude information (^) (Kutas et al ., 1990). Thus, like neurologically intact observers, concerning spatial locations can be cross-integrated (^) the attentional system of split-brain patients is unifocal. They (Trevarthen, 1968; Trevarthen and Sperry, 1973; Holtzman, (^) cannot prepare for events in two spatially disparate locations. 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 Attentional resources are shared
the task required the subject to move his eyes to the (^) Even though there seems to be but one focus of attention, highlighted point within the visual field stimulated. In the (^) the dramatic effects of disconnecting the cerebral hemispheres second condition, the subject was required to move his eyes (^) on perception and cognition might suggest that each half- to the relevant point in the opposite visual field. Split-brain (^) brain possesses its own attentional resources. If this were subjects could do this at above-chance levels, perhaps because (^) true, one would predict that the cognitive operations of one of crude cross-integration of spatial information. This was true (^) half-brain, no matter what the difficulty, would have only a even if the grid was positioned randomly in the tested field. (^) 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
Spatial attention can be directed but not divided task A, fewer are available for task B. This model maintains
between the hemispheres that the harder one hemisphere works on a task, the worse
The finding that some type of spatial information remains the other hemisphere does on a task of constant complexity. integrated between the two half-brains raises a question: are Many investigations have focused on this issue; all confirm the attentional processes associated with spatial information the notion that the central resources are limited (Holtzman affected by cortical disconnection surgery? Using a and Gazzaniga, 1982; Reuter-Lorenz et al ., 1996). In the modification of a paradigm developed by Posner and original experiment, two series of geometrical shapes were colleagues (Posner et al. , 1980) that capitalizes on priming displayed concurrently to the left and right of central fixation
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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
Fig. 7 An experiment showing that common, and therefore separated half-brains
limited, cognitive resources are available to split-brain subjects. The figure shows the sequence of events for a redundant three- While the resources a brain commits to a task appear constant, condition trial. Two series of geometrical shapes were shown their method of deployment can vary. The more items to be concurrently to each hemisphere, followed by a unilateral probe. analysed in a visual array, the longer it takes. After a baseline Split-brain patients were faster to decide whether the probe was (^) reaction time has been established it takes normal controls presented in the series when the non-probed hemisphere had been (^) an additional 70 ms to respond to two more items, another shown only one shape than when it had been shown several different shapes (adapted from Holtzman and Gazzaniga, 1982). 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, administered to a split-brain patient and normal controls; the reaction time to added stimuli is cut in half (Fig. 8) critical information was presented in each visual half-field (Luck et al ., 1989, 1994). (Holtzman and Gazzaniga, 1985). For normal subjects, the This notion was extended by Kingstone and colleagues visual information was automatically combined and perceived when they discovered that the strategy differs according to as one large problem. For the split-brain patient, each which hemisphere examines the contents of its visual field hemisphere perceived a problem that remained separate from (Kingstone et al. , 1995). The left-dominant hemisphere uses the perceptual information presented to the other half-brain; a ‘guided’ or ‘smart’ strategy whereas the right hemisphere thus, each hemisphere perceived a much simpler task. The does not. This means that the left hemisphere adopts a helpful results were clear: the split-brain patient outperformed the cognitive strategy in solving the problem whereas the right normal subjects. The callosum-sectioned patient benefited hemisphere does not possess those extra cognitive skills. But from the fact that the perceptual array under one of the test it does not mean that the left hemisphere is always superior conditions did not seem to be more difficult because the to the right hemisphere in attentional orienting. work was distributed to each separate hemisphere, even Kingstone and colleagues have demonstrated that the right though the sensory array was identical to that experienced hemisphere, which is superior to the left hemisphere for by the normal subjects. processing upright faces, shifts attention automatically to There is no question that disconnection of the cerebral where someone is looking (Kingstone et al. , 2000). The hemispheres allows a unique cognitive state. In a sense it left hemisphere does not demonstrate a similar attentional turns a unified perceptual system into two simpler perceptual response to gaze direction. systems that do not interact and therefore do not interfere The act of independent scanning in the hemispheres of with each other. It allows the breaking down of a large split-brain patients during visual search appears contrary to perceptual problem into smaller, more manageable problems the sharing of attentional resources. At this time, this issue that a half-brain can solve. From the observer’s point of remains unresolved and more research is needed. However, view, though, it looks as if the patient’s total information it should be mentioned that this apparent discrepancy may processing capacity has increased and is superior to that of reflect the fact that multiple mechanisms of attention appear
Callosum and cerebral specialization 1303
Fig. 8 Bilateral ( top left ) and unilateral ( bottom left ) search arrays with set size equal to 16. Bilateral (‘standard’) search and unilateral (‘guided’) search response times for split-brain patient J.W. (‘Experimental’, top panel ) and the normal control group ( bottom panel ) as a function of visual field and set size. Patients V.P. and D.R. showed the same results as J.W. (adapted from Kingstone et al ., 1995).
to operate at different stages of processing, some of which (Kingstone et al ., 1995). Mangun and colleagues have also might be shared across the disconnected hemispheres and shown that the right hemisphere has a predominant role in others of which might be independent (Luck and Hillyard, attentional orienting (Mangun et al. , 1994). Indeed, even in 2000). Luck and Hillyard describe evidence that the callosally sectioned patients, the right hemisphere attends to psychological refractory period paradigm reflects a late the entire visual field whereas the left hemisphere attends attentional mechanism, whereas visual search reflects an early only to the right field. This finding has also been noted by attentional mechanism. Berlucchi and colleagues (Berlucchi et al. , 1997) and by Corballis (Corballis, 1995).
Attentional orienting differs qualitatively
between the hemispheres Perceptual asymmetries following cerebral
Kingstone and colleagues have noted that the hemispheres disconnection
interact quite differently in their control of reflexive Hemispheric asymmetries in visuospatial processing have (exogenous) and voluntary (endogenous) attentional long been observed (e.g. Gazzaniga et al ., 1967). Never- processes (Enns and Kingstone, 1997; Kingstone et al ., theless, the fundamental nature of these asymmetries and 1997, 2000). The evidence suggests that reflexive attentional how they arose remain unclear. Initial studies with split-brain orienting happens independently in the two hemispheres, patients found that the right hemisphere outperformed the while voluntary attentional orienting involves hemispheric left at a variety of visuospatial tasks such as block design competition with control preferentially lateralized to the left and drawing three-dimensional objects (Bogen and hemisphere. These data explain not only the low-level sensory Gazzaniga, 1965; Gazzaniga et al ., 1965). These findings effects of attentional orienting but also bear on more complex contributed to the popular notion that the right hemisphere behaviours, such as visual search. For instance, when the is specialized for visuospatial processing. Subsequently, a number of items to be searched is small, attentional orienting number of researchers proposed dichotomies suggesting that is largely reflexive in nature, and the two hemispheres the two hemispheres process information in different, though perform independently (Luck et al ., 1989, 1994). But when complementary, ways. For example, Sergent suggested that the number of items to be searched is large, or the search the left hemisphere selectively processes the high-spatial- is strategic, attentional orienting is largely volitional and frequency information in a stimulus and the right hemisphere attentional orienting is lateralized to the left hemisphere selectively processes the low-spatial-frequency information
Callosum and cerebral specialization 1305
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
Fig. 10 Illusory contours reveal that the human right hemisphere^ et^ al .,^ 1993),^ which^ suggests^ that^ the^ grouping^ process can process some things better than the left. Both hemispheres (^) that is lateralized to the right hemisphere is not a recent can decide whether the illusory shapes ( left column ) are ‘fat’ or (^) evolutionary adaptation. This has led to the current ‘thin’. When outlines are added to the inducers so that the shapes (^) speculation that the right-hemisphere ‘specialization’ for can be perceived only by amodal completion ( right column ), only the right hemisphere can still tell the difference (adapted from visuospatial^ processing^ may^ be^ the^ result^ of^ the^ left Corballis et al ., 1999). hemisphere losing the visuospatial abilities it once possessed.
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’ There is a left-hemisphere matching deficit for
(Fig. 10). Performance is compared with that in a control visual stimuli
task in which the pacmen all face in the same direction and Recently, we have been studying the hypothesis that the left the participant is required to judge whether they are tilted hemisphere is capable of sophisticated visual processing but ‘up’ or ‘down’. Ringach and Shapley showed that represents spatial information relatively crudely compared neurologically intact observers are significantly better at the with the right hemisphere (Corballis et al ., 1999; Funnell shape discrimination task than the control task, which et al ., 1999). The implication of this hypothesis is that pattern indicates that the boundary-completion process assists in recognition is a function of both hemispheres but the right making the discrimination. The difference in performance hemisphere is further specialized for processing spatial between the two conditions provides an index of the information. Several recent results support this hypothesis. perceptual strength of the boundary completion. First, Funnell and colleagues discovered that the left The first experiment (Corballis et al ., 1999) investigated hemisphere of split-brain patient J.W. was impaired relative the generation of illusory contours by the isolated hemispheres to the right hemisphere in deciding whether two visually of two right-handed callosotomy patients, J.W. and V.P. presented objects were identical or mirror-reversed (Funnell Patient J.W.’s performance for both left-hemifield and right- et al. , 1999). This deficit was similar in magnitude for a hemifield stimuli was significantly improved by the presence variety of stimulus manipulations. In a follow-up study, of illusory contours. This indicates that J.W.’s two Corballis and colleagues (unpublished results) found similar hemispheres are equally capable of generating illusory left-hemisphere deficits in patients J.W. and V.P. for contours. Patient V.P. also showed improved discrimination judgements requiring spatial discriminations (size, orientation accuracy when illusory contours were present, although this and vernier acuity) but not for those requiring non-spatial was restricted to stimuli presented to the right hemifield. discrimination (luminance). This indicates that V.P.’s left hemisphere, at least, is capable Corballis and colleagues conducted a more explicit test of
1306 M. S. Gazzaniga
the hypothesis that the major difference in visual function motion. In contrast, more recent studies from three split- between the hemispheres is a right-hemisphere specialization brain patients (L.B., J.W. and V.P.) suggest a LVF/right- for representing spatial relationships (Corballis et al ., 1999). hemisphere advantage for the same judgement when the SOA They presented patients J.W. and V.P. with pairs of stimuli is long enough to support the perception of apparent motion within a single visual hemifield. These stimuli consisted of (Forster et al ., 2000). All these studies employed similar a square frame that contained a small icon in one corner. In methods. one condition (the ‘identity’ condition), the task was to judge The dissociation between the perception of apparent motion whether the icons were the same in each square. In the other and the detection of sequentiality was obtained within a single condition (the ‘spatial’ condition), the task was to judge patient (L.B.), which suggests that it cannot be accounted for whether the icons were in the same relative position in the by differences between subjects. The results imply that the two squares. There was a suggestion in the data that the left perception of sequentiality is performed better by the left hemisphere may perform the identity task better than the hemisphere, but that apparent motion, i.e. a more right, although both hemispheres performed this task well. ‘visuospatial’ phenomenon with a longer time constant, is In contrast, the right hemisphere was consistently better than perceived better by the right hemisphere. These findings are the left in the spatial condition. consistent with the notion that the left hemisphere has finer The results of this series of experiments indicate that temporal resolution than the right, as the percept of apparent the left hemisphere demonstrates striking deficits in simple motion, which may be lateralized to the right hemisphere, visuospatial tasks. It is noteworthy that experiments with requires a longer SOA than the discrimination of sequentiality, split-brained monkeys have sometimes revealed superiority which appears to be lateralized to the left hemisphere. of the left hemisphere for spatial judgements (e.g. Hamilton and Vermeire, 1991; Vogels et al ., 1994). The studies by
Funnell and colleagues (Corballis et al ., 1999; Funnell et al ., Monitoring and producing facial expressions
1999), as well as the preponderance of previous evidence
are managed by different hemispheres
from our laboratory and others, suggest that this is reversed (^) In the perceptual domain, it appears that the right hemisphere in humans. Although this difference should not be over- has special processes devoted to the efficient detection of interpreted, it is consistent with the idea that the evolution upright faces (Gazzaniga, 1989). Although the left hemisphere of language in the left hemisphere has resulted in the loss of can also perceive and recognize faces and can reveal superior some visuospatial abilities it once possessed. capacities when the faces are familiar, the right hemisphere appears to be specialized for unfamiliar facial stimuli (Levy et al ., 1972; Gazzaniga and Smylie, 1983). This pattern of
There are hemispheric differences in the asymmetry has also been shown for the rhesus monkey
(Hamilton and Vermiere, 1988).
perception of sequentiality and apparent motion
Since the right hemisphere is superior in the perception of When two spatially displaced visual stimuli are presented in faces, it would be reasonable to suppose it is also specialized rapid sequence, an observer may perceive a single stimulus for the management of facial expressions (Fig. 11). Recent moving between the two locations. This phenomenon is studies have shown, however, that while both hemispheres known as apparent motion. Whether apparent motion is can generate spontaneous facial expressions, only the perceived depends critically on the timing of the stimulus dominant left hemisphere can generate voluntary facial presentations. For example, Kolers has reported that the expressions (Gazzaniga and Smylie, 1990). It was also shown percept of apparent motion between successive flashes breaks that when the left hemisphere carried out a command to down at a stimulus–onset asynchrony (SOA) somewhere smile or frown, the right side of the face responded ~180 ms between 150 and 200 ms, given a spatial separation of 3.3° before the left side. This latter finding is consistent with the (Kolers, 1972). Nevertheless, subjects are typically able to fact that the callosum is involved in the execution of voluntary discriminate which of two flashes occurs first at much lower facial commands. SOAs (e.g. Corballis, 1996; Forster et al ., 2000). Thus, the perception of apparent motion can be dissociated from the ability to discriminate sequentiality from simultaneity. Recent
findings suggest that the neural representations of these Hemispheric specialization for sensory–motor
processes may also be dissociable. Rorden and colleagues tasks
have reported that parietal lesions that disrupt the judgement There are some tests that bring out hemispheric superiorities of successiveness can leave motion perception unimpaired in some of the patients. The block design test from the (Rorden et al. , 1997). In two recent papers, Corballis and Wechsler Adult Intelligence Scale is one such test. Here, the colleagues (Corballis, 1996; Corballis et al. , 2000) report a simple task of arranging some red and white blocks to match RVF/left-hemisphere advantage in sequentiality/simultaneity those of a given pattern results in the left hemisphere discrimination in one split-brain patient (L.B.) when the SOA performing poorly while the right triumphs (Bogen and was below the threshold for the perception of apparent Gazzaniga, 1965). However, in other patients both
1308 M. S. Gazzaniga
hemispheres. Surgical patients where callosal section is either limited or where there is inadvertent sparing of a part of the callosum enable one to examine functions of the callosum by region. For example, when the splenial region (posterior area of the callosum that interconnects the occipital lobe) is spared, there is normal transfer of visual information between the two cerebral hemispheres (Fig. 13). In such instances, pattern, colour, and linguistic information presented anywhere in either visual field can be matched with information presented to the other half-brain. Yet such patients do not transfer stereognostic information, and they also display a left ear suppression to dichotically presented auditory stimuli. Such observations are consistent with other human and animal data which reveal that the callosum’s major subdivisions are organized in functional zones where the posterior regions are more concerned with visual information; the anterior regions
Fig. 12 Sample Lissajous figures used to test anorthoscopic shape transfer auditory and tactile information (Hamilton, 1982; perception in each hemisphere. These stimuli were presented to (^) Gazzaniga, 1989). each hemisphere, moving behind a narrow slit so that only part of the figure was visible at any time, and the representation of the shape had to be constructed over time. Both hemispheres of
patient J.W. were capable of perceiving shapes in this fashion The anterior callosum is involved in higher-
(adapted from Fendrich et al. , 1996).
order transfer of semantic information
Patients who have undergone staged callosal section have
identifiable figure and then selected the figure from eight also provided glimpses into what the anterior callosal regions pictures inspected in free viewing conditions. The number transfer between the cerebral hemispheres. When the posterior of correct choices and the time required to attain correct half of the callosum is sectioned, the transfer of visual, figure percepts was recorded. The result was that both tactile and auditory information is severely disrupted, but the hemispheres could generate anorthoscopic percepts, the right remaining intact anterior callosum can transfer higher-order hemisphere having only a minimal advantage. Thus, the information. In one study the corpus callosum was sectioned synthesis of anorthoscopic figures occurs at a low level in in two stages (Sidtis^ et al ., 1981). After the^ first stage of the cortical visual processing hierarchy, where the processing sectioning the posterior callosum, the patient was unable to of visual information does not depend on lateralized name stimuli presented to the right hemisphere. Over a 10- mechanisms. week period, though, he began to name some stimuli. Upon close inspection of this capacity it was discovered that the right hemisphere was transmitting to the left hemisphere
Partial callosal section reveals specificity of gnostic cues about the stimulus but not the actual stimulus
commissure function (Fig. 14). In short, the anterior callosum transfers gnostic
In animal studies, sectioning the entire corpus callosum and (^) representations of the stimulus rather than the real stimulus. anterior commissure prevents the interhemispheric transfer (^) After section of the anterior callosum, this capacity ceased. of a wide range of modal and motor information. Partial sectioning of the commissures could also prevent some functions transferring across the callosum (Black and Myers,
1966; Sullivan and Hamilton, 1973; Hamilton and Vermeire, Callosal specificity for orthographic transfer
1988). In humans, comparable studies were not possible until Patient V.P. experienced inadvertent sparing of a band of we found patients who had not undergone full callosal fibres in the splenium and rostrum. These splenial^ fibres, section; when we found them it became apparent that specific seen in MRI, are functionally active in electrophysiological regions of the callosum were responsible for transferring experiments and early behavioural experiments (Gazzaniga specific types of information. This work was enhanced et al ., 1989; Mangun^ et al ., 1991). Funnell and colleagues when MRI enabled investigators to describe cut and uncut (Funnell^ et al ., 2000 a ,^ b ) report that, while there is no fibre systems. evidence for transfer of colour, shape, or size information, there is robust evidence for transfer of words presented visually. This is consistent with research by Suzuki and colleagues, who
MRI-verified lesions of partial sections reveal report dissociation between the interhemispheric transfer of
modal functions word and picture information (Suzuki et al. , 1998). They
When the corpus callosum is fully sectioned, there is little speculate that transfer of word information is supported by or no perceptual or cognitive interaction between the fibres in the ventroposterior region of the splenium, which
Callosum and cerebral specialization 1309
Fig. 13 Spared fibres in the corpus callosum allow the modality-specific transfer of perceptual and cognitive information. Patient J.KN. had some spared fibres in the splenium and was able to transfer visual information easily but performed at chance level for tactile information. Patient E.B. had a posterior callosotomy only, and was able to transfer sensorimotor information in one direction but not the other. This suggests that the neural fibres involved in transmitting the motor information to the opposite hemisphere were sectioned for only one direction of transfer. In contrast, patient J.W., who has a complete callosotomy, was unable to transfer any sensorimotor information. Patient V.P. has spared fibres at both ends of the corpus callosum. She is able to transfer some information about visually presented words from one hemisphere to the other, but otherwise appears fully split. For example, she is able to determine whether bilaterally presented words rhyme only if the two words look and sound alike (RL), but performs at chance level for all other conditions.
is the same region in which V.P. has callosal sparing (Fig. unaffected they appear to be in their general cognitive 15). The results for patient V.P. support the claim that awareness, affect and sense of self (Gazzaniga, 1970). At a remarkable functional specificity resides within the corpus superficial level of observation, separating half of the callosum. V.P.’s spared splenial fibres appear to support the neocortex from the other half appears to have little effect on transfer of word information but not visual information. cognition. Verbal IQ remains intact, as do within-hemisphere reaction times to perceptual stimuli and problem-solving capacity. Yet standardized memory tests administered
Memory studies after cerebral disconnection postoperatively hint at an impairment of short-term memory
The most powerful impression one has when observing (Zaidel and Sperry, 1974). Recent studies have extended patients who have had their hemispheres divided is how these observations.
Callosum and cerebral specialization 1311
Fig. 15 Patient V.P., who has spared fibres at both ends of the corpus callosum, is able to integrate words presented to both visual fields to create a concept that is not suggested by either word. For example, when presented with the words ‘head’ and ‘stone’ she combines the information presented in the separate fields into the integrated concept of a tombstone (top panel). In contrast, patient J.W. (bottom panel) is unable to integrate information from the two visual fields. When presented with the words ‘sky’ and ‘scraper’ he simply draws a picture of the sky and of a scraper in serial order (adapted from Kingstone and Gazzaniga, 1995 and Funnell et al ., 2000).
in most people (Kutas et al ., 1988; Petersen et al ., 1988; hemisphere’s because of its much lower rate of false alarms. Metcalfe et al ., 1995). These processes include, but are not The right hemisphere’s episodic memory is much more limited to, word and object knowledge, semantic elaboration veridical in nature (Phelps and Gazzaniga, 1992; Metcalfe and judgements, and semantic priming (Warrington and et al ., 1995; Miller et al ., 1998). It is as if the right Shallice, 1984; Demb et al ., 1995; Patterson and Hodges, hemisphere’s episodic memory is intact but its semantic 1995). Despite the left hemisphere’s superiority in semantic memory is impaired. processing, however, the left hemisphere also appears to be Studies of split-brain patients, therefore, provide support inferior in episodic memory tasks. This impairment is revealed for the distinction between semantic and episodic memory in the high rate of false alarms in the left hemisphere as (Fig. 16). These hemispheric memory dissociations are not opposed to the right hemisphere for semantically related true double dissociations in that one system is present and material (Phelps and Gazzaniga, 1992; Metcalfe et al ., 1995). another is not; rather, the one system is relatively impaired It is as though the left hemisphere has impaired episodic while the other remains relatively intact. As I point out in memory but intact semantic memory. the next section, episodic memory may be functioning quite Conversely, the right hemisphere is poor at semantic tasks well in each hemisphere, but its form or the nature of the even though it can have a robust lexicon and an intact representations may depend on the output of earlier systems. episodic memory system (Gazzaniga et al ., 1962, 1965; Gazzaniga and Sperry, 1967; Baynes et al ., 1992; Metcalfe
et al ., 1995). Despite the right hemisphere’s deficit in semantic Some hemispheric encoding asymmetries are
processing (i.e. simple problem-solving; LeDoux et al .,^ material-specific and some are independent of
1977 a ; Gazzaniga and Smylie, 1984), it recognizes words, material
pictures and abstract figures. Further, its performance in an The preceding research suggests a hemispheric difference in array of episodic memory tasks is often better than the left semantic and episodic memory. It has been further suggested
1312 M. S. Gazzaniga
Fig. 16 Schematic drawing showing how the left hemisphere differs from the right in mnemonic functions. The left is specialized for semantic processing while the right appears to be specialized for episodic memory.
that within episodic memory, there is a hemispheric difference callosum is severed is that they do not demonstrate significant between encoding and retrieval. The memory model HERA deficits in memory. What does the split-brain patient reveal (Hemispheric Encoding/Retrieval Asymmetry) proposed by about the neural substrates of memory processes? Tulving and colleagues (Tulving et al. , 1994) suggests A recent neuroimaging study suggests that the fundamental that episodic encoding is predominantly a left-hemisphere hemispheric difference in memory may be the nature of the function while episodic retrieval is predominantly a right- to-be-remembered material. Kelley and colleagues found that hemisphere function. Semantic retrieval, however, is thought words produced activations in the left prefrontal cortex, to rely on left-hemisphere regions. The model is based on nameable objects produced bilateral activations in the examination of activations in PET and functional MRI (fMRI) prefrontal cortex and faces produced activations in the right investigations of memory functions (Kapur et al ., 1994; prefrontal cortex (Kelley et al. , 1998). This possibility has Demb et al ., 1995; Kapur et al ., 1996; Nyberg et al ., 1996; been investigated by looking for hemispheric differences in Cabeza et al ., 1997; Dolan and Fletcher, 1997; Buckner and memory for verbal and perceptual stimuli in split-brain Koutstaal, 1998). Although many neuroimaging studies have patients (Miller et al ., 1997). In one task, the patients’ two provided support for the model, the results of other studies hemispheres were tested for memory of previously presented have not been compatible with the model. words. In the study phase, the patients engaged in either a Because this model attributes specific memory functions shallow encoding task (whether the words contained the to the two hemispheres, the split-brain patient provides an letter ‘A’) or a deep encoding task (whether the word ideal opportunity to test aspects of the model. If episodic represented a living object). The left hemisphere benefited encoding and retrieval each rely on a different hemisphere, from the deeper encoding whereas the right hemisphere did then dividing the hemispheres should have a devastating not. This is consistent with the suggestion, arising from the effect on episodic memory. As already noted, however, one HERA model, that episodic memory is predominately a left- of the most striking things about patients whose corpus hemisphere function.
