Neuropsychologia 163 (2021) 108041 Contents lists available at ScienceDirect Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia Can the mind be split? A historical introduction Michael C. Corballis *, Paul M. Corballis School of Psychology, University of Auckland, Science Centre, 23 Symonds Street, Auckland Central, New Zealand A R T I C L E I N F O A B S T R A C T Keywords: Commissurotomy Consciousness Split brain Subcortical connections The idea that the mind might be composed of distinct conscious entities goes back at least to the mid-19th century, and was at first based on the bilateral symmetry of the brain, with each side seemingly a mirrorimage replica of the other. This led to early speculation as to whether section of the forebrain commissures might lead to separate, independent consciousnesses. This was not put to the test until the 1960s, first in commissurotomized cats and monkeys, and then in humans who had undergone commissurotomy for the relief of intractable epilepsy. Initial results did indeed suggest independent consciousness in each separated hemisphere, but later findings have also revealed a degree of mental unity, especially in some perceptual functions and in motor control. Some of these findings might be interpreted in terms of subcortical connections or external crosscuing, and also address questions about the nature of consciousness in a more concrete way. 1. Introduction "two minds" The idea that the two sides of the brain might sustain separate conscious minds can be traced to 1844, with the publication of the book The Duality of Mind, by the English physician Arthur Wigan. Based on the seemingly identical features of the two sides of the brain, he argued that they must operate as separate minds. He nevertheless thought that these two minds had to be coordinated through “exercise and moral cultiva­ tion,” and that failure to do so could lead to pathology. Lack of coor­ dination might explain such phenomena as déjà vu, with an experience recorded in one side of the brain felt to be familiar by the other side, but not actually recalled. The two minds might also alternate, giving rise to different “personae,” each unaware of the existence of the other, as later popularized in Robert Louis Stevenson’s (1886) thriller The Strange Case of Dr Jekyll and Mr Hyde. What purported to be a real-life example was described in Morton Prince’s (1906) book Dissociation of a Personality, the case of a Miss Beaumont who occasionally appeared in the person­ ality of a very different person known as Sally B. direita/esquerda Wigan did not attribute different mental qualities to the two sides of the brain. Based on the prevalence of right-handedness, though, he did suggest that the left side was generally “superior in power” to the right, which “aids the left and corroborates its fellow as an assistant aids a workman” (Wigan, 1844, p. 313). Broca’s (1861) later discovery of a left-brained dominance for speech, though, led to much speculation about fundamental differences between the two sides. For example, the French physician Gaetan Delaunay (1874) thought that the two sides NOT APPROVED direita/esquerda had different kinds of dreams, and that the left brain was associated with maleness and reason, and the right side with femaleness and emotion. VOID The historian Anne Harrington, 1985 remarks, “It is interesting that, once one has given the two hemispheres sexual identities, the idea of cerebral dominance becomes a rather apt metaphor for the social and economic domination of men over women in 19th-century Europe” (p. 624). Much of the dual-brain speculation evaporated after the turn of the century, but was revived in different guises following the split-brain studies of the 1960s. one mind It was also well understood in the 19th century that the two cerebral cortices were connected by several commissures, of which by far the largest and most important was the corpus callosum. This gave rise to early speculation as to what would happen if the corpus callosum were severed. The experimental psychologist Fechner (1860) argued that the mind would then indeed be split, and essentially duplicated, with each half carrying the same moods, predispositions, knowledge and mem­ ories. This was later challenged, though, by the British psychologist William McDougall (1911), a dualist who believed that the mind would remain unified even if the two halves were separated. He even asked the famous physiologist Sir Charles Sherrington to cut his corpus callosum if he were to contract an incurable disease. “If I am right,” he is reported to have said, “my consciousness will remain a unitary consciousness” (quoted by Zangwill, 1974, p. 265). In the first half of the 20th century, studies of damage to the corpus callosum provided some evidence as to its function, but little of conse­ quence to the understanding of what would happen if it were split. Based * Corresponding author. E-mail addresses: m.corballis@auckland.ac.nz (M.C. Corballis), p.corballis@auckland.ac.nz (P.M. Corballis). https://doi.org/10.1016/j.neuropsychologia.2021.108041 Received 21 November 2020; Received in revised form 20 August 2021; Accepted 12 September 2021 Available online 25 September 2021 0028-3932/© 2021 Published by Elsevier Ltd. M.C. Corballis and P.M. Corballis Neuropsychologia 163 (2021) 108041 1967; Gazzaniga et al., 1962, 1965). As in the 19th century, this again led to often extreme speculation as to fundamental differences between the two sides of the brain. Joseph E. Bogen (1989), one of the surgeons who carried out the split-brain operation, characterized the left brain as propositional and the right side as appositional, a duality elaborated by Ornstein (1972). Bogen supposed that the duality was evident even in the intact brain, and coined the term neo-Wiganism in recognition of Wigan (1844) earlier claims.1 The idea that the two sides of the brain process the world differently has gained some support. For example, Wolford et al., (2000) found that the two sides form different hypotheses as to what will occur next in a sequence of events, with left hemisphere seeking patterns in the se­ quences and the right hemisphere matching past frequencies. They take this as evidence for the left brain as the “interpreter,” generating hy­ potheses, whereas the right hemisphere relies on simple associations (Gazzaniga, 1995). Other evidence, though, suggests the right brain is the “interpreter” when it comes to visual processing (P.M. Corballis, 2003). More generally, the notion of a global difference, as proposed by Bogen and elaborated in popular views of “left-brain” and “right-brain” modes of thought, is an oversimplification. There are many respects in which the two sides of the brain operate in like fashion rather than differently (M.C. Corballis, 2020), and where differences occur they are not on a single continuum, but rather occur on several independent dimensions (Häberling et al., 2016; Liu et al., 2009). The discovery of specialized processing within the hemispheres need not mean that they are separately conscious. Sperry’s Nobel Prize was “for his discoveries concerning the functional specialization of the ce­ rebral hemispheres,” but his more dramatic claim was that the discon­ nected hemispheres function as separate minds, in apparent denial of McDougall’s dualism. In a lecture delivered in Stockholm when he received his prize, and later published in Science, Sperry (1982) sum­ marized as follows: on the effects of callosal tumors, Raymond et al. (1906) described what they called a mental callosal syndrome, involving a loss of connectedness of ideas, problems of recent memory, a bizarreness of manner, and swings of mood. However, it was difficult in individual cases to distin­ guish effects of callosal damage from those of neighboring damage, although the surgeon Walter Dandy in 1936 reported on a case in which the corpus callosum was split in an operation to remove a pineal tumor and wrote that " … no symptoms follow its division. This simple experiment puts an end to all of the extravagant hypotheses on the functions of the corpus callosum” (Dandy, 1936, p. 40). In the 1940s, William van Wagenen, a surgeon in Rochester NY, severed the corpus callosum for the relief of epilepsy in a series of pa­ tients, and examination by the psychiatrist Andrew Akelaitis did in fact reveal some of the psychological effects that were later to attract widespread interest (Akelaitis, 1941, 1942, 1945; Akelaitis et al., 1942), but at the time these did not seem to attract interest. Although epileptic seizures were relieved in seven of the 10 patients, the operation was not considered successful enough to warrant continuation, and in a review of the evidence Tomasch (1954) concluded that "’the corpus callosum is hardly connected with any psychological function” (p. 119). Things changed dramatically in the 1960s. 2. The California series Roger W. Sperry began his split-brain research using cats and mon­ keys. By splitting the optic chiasm as well as the corpus callosum, he and his colleagues were able to present visual information to one side of the brain by presenting it to just one eye. A visual input to the left eye would therefore be projected only to the left brain, and input to the right eye only to the right brain. The results revealed remarkable disconnections. If the split-brain animal learned to make a visual discrimination, such as responding to a cross but not to a circle, when viewing with one eye, it was then unable to make that discrimination when tested with the other eye. Each side of the brain could even be taught conflicting discrimi­ nations, with one eye and therefore one side of the brain learning to respond to a cross but not to a circle, and the other eye–brain combi­ nation learning the opposite. In monkeys, by using polarized filters, conflicting information could be presented to the two eyes simulta­ neously, and the animal learned both discriminations without any apparent conflict. When later given a free choice, the animals would alternate periodically between the two, as though each side of the brain would take control for a while before yielding to the other. As Sperry (1961) put it, “The split-brain cat or monkey is thus in many respects an animal with two separate brains that may be used either together or in alternation” (p. 133). Michael S. Gazzaniga was aware of split-brain surgery on humans for the relief of epilepsy, and became interested in testing whether humans might show similar dissociations. He at first approached van Wagenen in Chicago, but this initiative failed, and he then enrolled as a PhD student in Sperry’s laboratory. Two Los Angeles surgeons, Philip J. Vogel and Joseph E. Bogen, spurred by Sperry’s earlier work on cats and monkeys, decided again to sever the corpus callosum, along with the anterior commissure and hippocampal commissure, for the relief of intractable epilepsy. This time, the operation was judged successful, and has been repeated in a number of settings around the world, typically with section of the corpus callosum alone, and with decreasing frequency due to more effective alternative treatments. Gazzaniga and Sperry, aided by Bogen, seized the opportunity to examine these patients, with a view to determining the extent to which the two hemispheres operated independently. For obvious ethical rea­ sons, it was not feasible to section the optic chiasm in human patients, but Gazzaniga and Sperry were able to project information to a single hemisphere by flashing it quickly in one visual hemifield, or by having shapes felt by one hand. They soon established a left-hemisphere dominance for speech along with some evidence of right-hemisphere specialization for nonverbal processing (e.g., Gazzaniga and Sperry, Each disconnected hemisphere behaved as if it were not conscious of cognitive events in the partner hemisphere … Each brain half, in other words, seemed to have its own largely separate cognitive domain with its own private perceptual, learning, and memory ex­ periences, all of which were seemingly oblivious to corresponding events in the other hemisphere. (p. 1224). Separate consciousness within each disconnected hemispheres was implied in a study by Luck et al. (1989). In searching for a specified target in visual arrays that covered both visual fields, two split-brain patients scanned twice as quickly as did control participants, implying that they undertook separate but simultaneous searches in each hemi­ sphere. Independent consciousness is also implied by the phenomenon of the “alien hand” (Feinberg et al., 1992). For a period after the com­ missurotomy, the patient’s nondominant hand may act in opposition to what the patient intends with the dominant hand; Gazzaniga et al. (1962) note such instances, as when the right hand picks up the evening paper, the left hand puts it down, and the right hand picks it up again. They write: It was as if the control of the left hand were strongly centered in the minor hemisphere at such times and hence isolated from the main intent and prevailing directorship of the dominant hemisphere (p. 1267). Because this implies an element of intention, Bogen (1993) has preferred the term “anarchic hand.” There are also occasional indications that patients do transfer in­ formation between hemispheres. In one study, the patient L.B. seemed 1 Bogen also arranged for Wigan’s book to be republished in 1985, and owned a car with the licence plate WIGAN. 2 M.C. Corballis and P.M. Corballis Neuropsychologia 163 (2021) 108041 able to name digits projected to the left hemifield (and right hemi­ sphere), and had also been shown to recognize rhymes shown to the left hemifield (Zaidel and Peters, 1981). Myers and Sperry (1985) charac­ terized the transferred information as " … neither precise nor complete nor unprocessed. It appears to consist rather of limited arousal or orientational cues and partial, contextual or ambient impressions anal­ ogous to ‘mental block’ or ‘tip of the tongue’ sensations in which there is available some relevant information which is yet insufficient to trigger precise identification” (p 256). It was also possible that the patient L.B. had limited speech in the right hemisphere, so his ability to give verbal responses to digits in the left hemifield need not imply transfer. Another study revealed L.B., along with two other patients, to be unable to judge whether digits, letters, line drawings of faces, and colors flashed on either side of the vertical meridian were the same or different (Johnson, 1984). A fourth patient (N.G.) did show ability to make these decisions, as she again did a study by Myers and Sperry (1985), but in later studies she was also at chance, as were two other patients (M.C. Corballis, 1994; Corballis and Corballis, 2001). The occasional ability of patients to make interhemi­ spheric comparisons may be due in part to cross-cueing, or to imperfect control of visual fixation, but the results generally show little if any ability to judge input in opposite hemispheres to be same or different. Nevertheless, it has long been observed that split-brained patients maintain a sense of unity in their everyday lives, further hinting that consciousness may not be quite so divided as originally claimed. Bogen (1993) wrote of their “social ordinariness” (p. 3), and Sperry (1968) remarked that “a person with complete section of the forebrain com­ missures would usually go undetected as a rule in a casual first meeting or conversation or even through an entire routine medical exam” (p. 1223). It was perhaps observations such as these that led to earlier be­ liefs that the corpus callosum was of little importance to psychological function. Sergent (1987) showed that split-brained patients were well above chance at deciding whether sloping lines in the two hemifields were aligned or not, or whether an arrow in one field pointed to a dot in the other, again suggesting subcortical processing of location and orienta­ tion. Such results suggest that subcortical processing is not restricted to peripheral vision or to prolonged viewing, as suggested by Trevarthen and Sperry (1973). There is other support for the integration of motion perception across hemifields. Ramachandran, Cronin-Golomb and Myers (1986) reported that three patients perceived apparent motion when a light presented in one hemifield was followed by a light in the other. This was later confirmed in a study with added controls designed to rule out inferential strategies (Naikar and Corballis, 1996). Another study showed that a line-motion illusion (Hikosaka et al., 1993) triggered by a flash of light was induced when the flash and perceived motion were in opposite hemifields (M.C. Corballis et al., 2004). The corpus callosum itself is a structure limited to eutherian mam­ mals, and was preceded phylogenetically by other commissures, including the anterior commissure and various subcortical commissures including the tectal commissure connecting the superior colliculi. Interhemispheric transfer seems well developed in non-eutherian spe­ cies such as birds (e.g., Manns et al., 2017) and fish (e.g., Hemsley and Savage, 1987). One possibility is that the corpus callosum enables interhemispheric integration of higher-order cortical functions such as object recognition and language, while subcortical systems have to do with more basic visual functions such as visual attention, and the perception of location, orientation, and movement. The collicular sys­ tem may play a regular role in mammals, and link to cortical areas, as suggested by Trevarthen and Sperry (1973). Based on her own findings, Sergent (1987) wrote as follows: This subcortical coordination of hemisphere activity may thus un­ derlie the behavioural integration displayed by commissurotomized patients in their daily activities, allowing them to relate different parts of the visual field and to maintain a unity of purpose in their action (p. 1389).2 3. Subcortical transfer? Trevarthen and Sperry (1973) had also suggested that visual transfer might be accomplished subcortically through what they called the ambient visual system, as distinguished from the cortical focal system. While the focal system was dedicated primarily to vision in the foveal region and dedicated to detailed vision and the recognition of objects, the ambient system is sensitive to peripheral vision and to moving stimuli. It is largely subcortical, involving projections via the superior colliculus to the pulvinar nucleus of the thalamus, where it interacts with visual association areas of the cortex (e.g., Ingle, 1967; Schneider, 1967). This system has also been referred to as the “second” visual system (Bogen, 1990). To demonstrate the role of the ambient system in interhemispheric transfer, Trevarthen and Sperry (1973) moved large shadowcast stimuli into peripheral vision and required the subjects to hold fixation while they viewed them. Three split-brained patients were able make quite accurate judgments about the relative motion of disks and lines located some 45◦ from fixation in the two hemifields, and were also able to make crude verbal statements about stimuli in the left hemifield. They also responded quite well to changes in size and brightness, but descriptions of shapes were poor, although they could describe simple properties such as whether a shape was elongated or square, or whether it was single or composed of two parts. The subjects could also crudely identify colors in the left hemifield, at a level approximating that of a dichromat. Later studies also showed transfer of motion, location, and control of spatial attention, functions thought to be processed in the superior colliculi. Holtzman (1984) found that split-brain patients could direct an eye movement to a specific location in one visual hemifield on the basis of a locational probe flashed briefly in the other, but could not do so if the probe was a shape rather than a location; for example, if the probe was a cross, the patients were unable to move their eyes to the cross in a 2 × 2 matrix that also contained a circle, a square, and a triangle. In that respect, split-brain patients appear to be of one mind, rather than two. Savazzi et al. (2007) provided an elegant demonstration of the role of the superior colliculus in cross-hemispheric transfer. Simple reaction time is longer when the signal is on the side opposite the responding hand (Poffenberger, 1912), and this effect was considerably prolonged in split-brained patients when the signal was presented in short-wavelength light undetectable by superior-colliculi neurons. This effect was not evident in individuals with intact commissures. The findings to this point seemed to suggest that the two hemispheres do sometimes function as separate conscious entities, but also sometimes combine in a unified manner. To the extent that it occurs, separate consciousness in the two hemispheres seems to rule out theories that propose a global workspace (e.g., Baars, 2005; Dehaene and Naccache, 2001) or an integration across different circuits (e.g., Tononi and Koch, 2015). They support instead the view that consciousness depends on local recurrent circuits (e.g., Block, 2007; Lamme, 2006), which can be contained within one or the other hemisphere. This further implies that consciousness need not be accessible to speech, as when conscious be­ haviors are initiated by the right hemisphere. In the case of Sperry’s earlier experiments on cats and monkeys, of course, neither hemisphere could produce speech, and there still seemed clear evidence of inde­ pendent consciousness in the two hemispheres. In some cases, though, split-brain patients do behave in integrated fashion. This might involve cases where existing commissures, such as 2 Justine Sergent took her own life in 1994, which may have dampened in­ terest in her findings. Her main findings on the split-brain, though, have been largely confirmed (M. C. Corballis, 2016). 3 M.C. Corballis and P.M. Corballis Neuropsychologia 163 (2021) 108041 the tectal commissure, retain a degree of sensory and perhaps emotional and semantic integration. Integration sometimes takes time to emerge, as when the alien hand ceases to emerge and patients begin to display more of what Bogen called “social ordinariness.” Patients may also develop integrated strategies, such as cross-cuing. That is, each hemi­ sphere can signal to the other externally. One hand may touch the other, or visibly tap a finger so that either hemisphere can see it. Even directing gaze to particular objects or scenes can alert one hemisphere to what is being processed by the other. Interest in the split brain gradually diminished over the past half century, as effective alternative treatment for epilepsy were developed, and fewer cases of commissurotomy were available. Against this trend, though, was a flurry of interest in the late 2010s, and it was this that prompted this special issue. Whether a parallel system operates in primates remains to be seen. There may be truth to all of these accounts, and the question remains not so much that of whether consciousness is divided in the split brain as of when it is divided and when it is not. As de Haan et al. (2020) point out, this must depend in part on what defines consciousness – there are certainly some respects in which processing is divided in the split brain and some in which they are not. Precise description of the varying ca­ pacities of split-brain patients should help us understand what con­ sciousness is – or perhaps question whether we really need the concept at all. References Akelaitis, A.J., 1941. Studies on the corpus callosum: II. The higher visual functions in each homonymous field following complete section of the corpus callosum. Arch. Neurol. Psychiatr. 45, 788–796. Akelaitis, A.J., 1942. Studies on the corpus callosum: V. Homonymous defects for color, object and letter recognition (homonymous hemiamblyopia) before and after section of the corpus callosum. Arch. Neurol. Psychiatr. 48, 108–118. Akelaitis, A.J., 1945. Studies on the corpus callosum: IV. Diagnostic dyspraxia in epileptics following partial and complete section of the corpus callosum. Am. J. Psychiatr. 101, 594–599. Akelaitis, A.J., Risteen, W.A., Herren, R., van Wagenen, W.P., 1942. Studies on the corpus callosum: III. 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Revival The renewed interest began with a claim by Pinto et al., (2017a, b) that consciousness is unified in the split brain, but perception is divided. They based this on a split-brained patient who could respond with either hand or verbally to the location, orientation or identity of an object across the entire visual field, but were unable to compare stimuli across hemifields. Because the patient could respond with either hand and claimed awareness of the entire visual field, the authors suggested that he retained unitary consciousness. With perception divided, the ques­ tion is then how consciousness is unified. Following from the study by Pinto et al., 2017a, 2017b, de Haan et al. (2021) suggest that, in the normal brain as in the split brain, conscious perception can be localized in independent circuits, but that the impression of unity depends on the fact that the body itself is a single entity in an external world with ever-changing constraints. The apparent singularity of consciousness then resides in the execution and planning of bodily action. Volz and Gazzaniga (2017) responded to the article by Pinto et al. (2017a, 2017b) by retaining the strong view that consciousness is indeed divided in the split brain, but that when interhemispheric transfer is seen to occur, it may be achieved through cross-cuing, as suggested earlier. Even facial expressions might serve as informational cues. Volz and Gazzaniga also suggest that mirror neurons within each hemisphere may play a role, enabling one hemisphere to perceive the goal of an action produced by the other (Rizzolatti and Sinigaglia, 2010). If the two sides of the brain do indeed have separated minds, they have shared the one body, and it would not be surprising if they had devised intimate strategies for communication. M. C. Corballis et al. (2018) reiterated the possible role of subcortical exchange between hemisphere, as reviewed earlier, in establishing at least a degree of visual unity between hemispheres in the split brain. Pinto and colleagues do recognize this possibility, but suggest that their results probably do not depend on the anterior or posterior commissures. These structures were intact in the patient they investigated, but had been severed along with the corpus callosum in a number of earlier patients, and disconnection effects seem to be independent of whether or not they are intact. This has little bearing, though, on the role of the collicular system, because the tectal commissure, which connects the superior colliculi appears to have been unaffected in the patients tested in the Californian series, as well as in subsequent patients. The collicular system is likely to have remained functional bilaterally in all split-brain patients so far examined. 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