Principles of Human Brain Organization Derived From Split-Brain Studies (Gazzaniga 1995)

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Principles of Human BrainOrganization Derived fromSplit-Brain StudiesReview

Michael S. Gazzaniga

Center for NeuroscienceUniversity of California, DavisDavis, California 95616Studies of damaged human brains have always intriguedneuroscientists. The rich symptomatology that can resultis riveting to all who experience examination of such pa-tients. Yet, one of the concerns of basic scientists is thatstructure-function correlates are difficult to make in thedamaged brain, since the lesions are naturally occurringand usually quite diffuse. In addition to the problem ofquantitating the lesion, there has always been concernwhether the information gained about the brain in the pres-ence of lesions is all that useful in understanding normalbrain mechanisms. Are observed effects due to the dam-age of specific areas or to distant effects? These and otherissues have limited the general acceptance of the findingsfrom clinical studies.One of the immediate appeals of the study of patientswith surgical division of the forebrain is that the separatefunctions of the two cerebral hemispheres can be studiedreadily in the absence of focal damage. Also, the callosalsurgery, while producing damage to the brain, was dis-crete damage to a fiber system and not to nuclear areas.In 1961, R. W. Sperry and his colleagues commenced aseries of studies on patients who had undergone surgicalsection of the cerebral commissures in an effort to controltheir otherwise intractable epilepsy (Bogen et al., 1965).Studies continue on the original patients as well as othersand still shed light on the nature of both cortical and sub-cortical neural networks. In what follows, I review someaspects of this work to illustrate how this initial work hasprogressed from the early sixties until the time of Sperry'sdeath in the spring of 1994.Patients who undergo so-called split-brain surgery allsuffer from intractable epilepsy. Prior to their surgery, ex-tensive attempts are made to control their seizures medi-cally. Failure to do so, along with other clinical criteria,finds them candidates for surgical division of the corpuscallosum, and in some cases the anterior commissure aswell. Although these patients are not normal, the onset oftheir epilepsy varies and has different etiologies. It hasnot been possible to correlate any of these variations intheir neurologic history with the pattern of results obtainedfrom the cognitive studies. It is known from other data that,in order for there to be significant changes in the normalpatterns of cerebral lateralization, a large lesion must oc-cur to one side of the brain in early childhood (Rasmussenand Milner, 1977).In the original studies on the California series of patients,it was necessary to rely on surgical notes for determinationof the completeness of the surgical sections. In more re-cent years, both magnetic resonance imaging (MRI) andother electrical brain mapping techniques have provided amore accurate representation of the extent of the surgicalsections. Accu rate documentation of the extent of callosalsection becomes crucial for understanding the organiza-tion of the cerebral commissure.The main methods of testing the perceptual and cogni-tive functions of each hemisphere have not changed inprinciple over the years. However, there have been signifi-cant advances in the technologies used to present stimulito the surgically separated hemispheres. In the earlyyears, information was visually lateralized to one or theother hemispheres by quickly flashing stimuli to one orthe other visual field using electronic shutters attached toslide projectors (see Figure 1). As the patient fixates ona point in space, information flashed to the left of fixationis presented exclusively o the right hemisphere. The quickflashing is necessary to control for unwanted eye move-ments, which would redirect the information into the un-wanted hemisphere. This method has been replaced byusing computer-based stimuli presentation arrangements.More importantly, the development of an image stabilizingsystem, used in concert with a Purkinje eye tracker, nowpermits sustained presentation of information to either vi-sual field, and therefore, either hemisphere. Accordingly,if a subject moves his or her eyes away from fixation, thestabilizing system moves the stimulus with the eyes andthereby prevents the information from being presented tothe wrong hemisphere. This technological developmenthas allowed for new findings on both the neurological andpsychological aspects of hemisphere disconnection.

Fundamental Principles Arising from Initial Studies

The original reports on the California series of patientsdealt with a number of fundamental issues concerning thebasic psychological properties of the separated cerebralhemispheres, as well as basic issues of neurological orga-nization (Sperry et al., 1969; Gazzaniga, 1970). In manyrespects, the issues raised in the original studies still drivecurrent research efforts. In the following, the neurologicconsequences will be reviewed first, followed by the stud-ies on the separate psychological properties of the twocerebral hemispheres.

Sensory and Motor Studies

The human studies were carried out in the context ofstrong new animal evidence, obtained by Myers andSperry (1958), that dividing the cerebral commissures pro-duced a profound deficit in the interhemispheric transferof sensory and motor information. In the cat, monkey, andchimpanzee, Myers (1956) had determined that, followingmidline section of the corpus callosum and anterior com-missure, visual and tactile information lateralized to onehemisphere did not transfer to the opposite hemisphere.This resulted in the so-called "split-brain" animal. This star-tling discovery was completely contrary to earlier reportson the effects of human commissure section reported byAkelaitis (1941, 1944). Akelaitis reported no significantneurological or psychological effects following section ofthe callosum.

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Figure 1. Stimulus LateralizationTechniqueTo examinedifferentiallyhemisphericprocessingdifferences, t is necessary to lateralizestimuli within the left and right visual fields (upperleft). However, f the subject makes an eye movementduring he stimu-lus presentation, proper ateralization s no longer maintained uppermiddle). Thus, retinal stabilization s useful o counteract he effectsof such eye movements upper ight).A dual Purkinje mage eyetrackercoupledwith a mirror stimulusdeflectorallowssuch etinalstabilization (lower eft).As eye movementsoccur, horizontaland verticaldeflection mirrors move o counteractsuch movements, maintainingproper ater-alization (lower right).The surgeries on the original California cases (W J, NG,and LB) were able to show that humans responded toforebrain commissurotomy in essentially the same way asthe monkey and chimpanzee. Visual information pre-sented to one half-brain was not available to the otherhalf-brain for analysis. A similar principle applies to touch.Objects placed in the right hand were normally namedand described, but objects presented in the left hand werenot. Similarly, sensory information presented to one hemi-sphere was useful in guiding the contralateral hand butvery ineffective in controlling the ipsilateral hand.From a cognitive point of view, the first studies confirmedlong-standing neurologic knowledge about the nature ofthe two cerebral hemispheres. The left brain was dominantfor language, speech, and major problem solving, whilethe right appeared specialized for visuospatial tasks suchas drawing cubes and other three-dimensional patterns.Of course, this meant that visual and tactile stimuli pre-sented to the right hemisphere could not be named ordescribed, since the sensory information was discon-nected from the dominant left speech hemisphere. Thisdramatic result stood in contrast to the right hemisphere'sability to acknowledge the presence of these stimuli byallowing it to respond in a nonverbal manner, such aspointing to matching objects and the like.In the subsequent 30 years, these studies have beenfollowed up by a nu mber of investigators. While the originalstudies set the framework for subsequent research, thehuge effort to characterize fully these unique human be-ings has continued to yield major insights into the organi-zation of the human brain.

Perceptual and Attentional Studies FollowingCerebral Disconnection

The attentional and perceptual abilities of split-brain pa-tients have been extensively explored. Visual perceptionis the easiest to study. Overall, following cortical discon-nection, perceptual information does not interact betweenthe two cerebral hemispheres, whereas the supportingcognitive processes of attentional mechanisms do some-times interact.

Simple Perceptual Interactions Are Not Seen

Split-brain patients are not able to cross-integrate visualinformation between their two visual half-fields. When vi-sual information is lateralized to either the left or right dis-connected hemisphere, the unstimulated hemispherecannot use the information for perceptual analysis (seeFigure 2). This is also true for stereognostic informationpresented to each hand. While the presence or absenceof touch stimulation is noted to any part of the body byeither hemisphere, patterned somatosensory informationis lateralized. Thus, an object held in the left hand cannothelp the right hand find an identical object. Although therehave been reports arguing that some higher order percep-tual information is integrated at some level via subcorticalstructures (Cronin-Golomb, 1986; Sergent, 1990), theseresults have not been replicated by others (Seymour etal., 1994; Corballis et al., 1993; Corballis, 1994; McKeeveret al., 1981).

Humans Show Visual MidlineOverlap Phenomenon

There is some nasotemporal overlap at the retinal verticalmeridian in cat and monkey (Stone, t966; Stone et al.,1973). In a stripe 1-2 degrees of visual angle wide thatstraddles the two visual half-fields, visual information issent to both the left and right visual cortices. Whether ornot the anatomical projections have any functional signifi-cance has never been examined in the animal. Fendrich etal. (1989) have examined this issue in split-brain patients.Using an image stabilizer combined with a Purkinje eyetracker, careful assessment of the visual midline of twosplit-brain patients has revealed an area of no more than2 degrees in width at the vertical midline where visualinformation appears available to each half-brain. This con-trasts with the findings of Sugishita et al. (1994), who foundno overlap but who were disadvantaged by not having theimage stabilizer to carry out their midline studies. Still,within this strip of overlap, the signals conveyed to eachhemisphere from the contralateral hemiretina appear tobe weak or degraded. Stimuli could not be comparedacross the vertical meridian if these comparison requireddetailed shape information, or if the stimuli were presentedfor only 200 ms.

Review: Human Split-BrainStudies219

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Figure 2. InterhemisphericTransfer TestsThe upperexampledepicts spatial ests. On within-field rials (A), theeyes moved o the stimulus that was surrounded by the probe. Onbetween-field rials (B), the eyes also moved o the correspondingstimulus in the other hemifield. n contrast, when perceptual nforma-tion was used as the cue (lower examples), he capacity o find thepatterned cue was only possibleon the within-field rials (A). On thebetween-field rials (B), the response o the opposite ield was only atchance.

Interhemispheric Transfer Is Seen for CrudeSpatial Location Information

Unlike visual and somatosensory

cues,

crude informationconcerning spatial locations can be cross-integrated(Trevarthen, 1968; Trevarthen and Sperry, 1973; Holtz-man, 1984). In one set of experiments, a four-point gridwas presented to each visual field. On a given trial, oneof the positions on the grid was highlighted, and one con-dition of the task required the subject to move his eyesto the highlighted point within the visual field stimulated.In the second condition, the subject was required tomove the eyes to the relative point in the opposite visualfield. Split-brain subjects were easily able to do this,thereby suggesting some crude cross-integration of spa-tial information. This was true even if the grid was randomlypositioned in the tested field.

Spatial Attention Can Be Directed but Not

Divided

between the Hemispheres

The finding that some type of spatial information remainsintegrated between the two half-brains raises the questionof whether the attentional processes associated with spa-tial information are affected by cortical disconnection sur-gery. Using a modification of a paradigm developed byPosner et al. (1980) that capitalizes on spatial priming phe-nomena, Holtzman et al. (1981) found that either hemi-sphere can direct attention to a point in either the left orright visual field. Posner first showed that the responselatency to a peripheral visual target is reduced when ob-servers have prior information regarding its spatial locus,even when eye movements are prevented. Presumably,the spatial cue allows observers to direct their attentionto the appropriate location prior to the onset of the target.When this paradigm was used in split-brain patients tomeasure the extent to which such attentional cues affectperformance, the separated hemispheres were found notto be strictly independent in their control of spatial orienta-tion. Rather, the two hemispheres rely on a common ori-enting system to maintain a single focus of attention. Thus,as with normal people, a cue to direct attention to a particu-lar point in the visual field is used no matter which hemi-sphere is presented with the spatial cue.The discovery that spatial attention could be directedwith ease to either visual field raised the question ofwhether each separate cognitive system in the split-brainpatient could, if instructed to do so, independently directattention to a particular part of its own visual field (Holtz-man et al., 1984). Can the right hemisphere direct attentionto a point in the left visual field while the left brain simulta-neously directs attention to a point in the right visual field?Normal subjects cannot so divide their attention. Can split-brain patients with evident cognition in both hemispheresdo so?Results from several studies show that the split-brainpatient s unable to divide spatial attention between the twohalf-brains. There would appear to be only one integratedspatial attention system that remains intact following corti-cal disconnection. Thus, like neurologically ntact observ-ers, the attentional system of split-brain patients is unifo-cal. They are unable to prepare for events in two spatiallydisparate locations.

Attentional Resources Are Shared

The dramatic effects of disconnecting the cerebral hemi-spheres on perception and cognition might suggest eachhalf-brain possessed its own attentional resources. If true,one would predict the cognitive operations of one half-brain, no matter what the difficulty, would little influencethe cognitive activities of the other. The competing viewis that the brain has a set of limited resources that managesuch processes, and if they are being applied to task A,there are fewer available for task B. This model wouldpredict that the harder hemisphere A worked on a task,the worse hemisphere B would do on a task of constantcomplexity.Many studies have been carried out on this issue, andall confirm the notion that the central resources are limited(Holtzman and Gazzaniga, 1982). In the original experi-ment, there were two conditions. In what was called the"mixed" or hard condition, two series of three different geo-metric shapes were displayed concurrently to the left andright of central fixation and thus were lateralized to theright and left hem spheres, respectively. In the"redundant"or easy condition, the series of three different geometricshapes was presented to only one hemisphere, while theother viewed three identical geometric shapes. A unilateralprobe figure subsequently appeared, and the observer in-dicated with a forced-choice key press whether it matchedany of the probed field's items. The results clearly showedthat, when one half-brain was working on processing only

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