Which of the following statements is true about the specialization of function in a hemisphere of the brain?

Abstract

Split-brain patients constitute a small subpopulation of epileptic patients who have received the surgical resection of the callosal fibers in an attempt to reduce the spread of epileptic foci between the cerebral hemispheres. The study of callosotomy patients allowed neuropsychologists to investigate the effects of the hemispheric disconnection, shedding more light on the perceptual and cognitive abilities of each hemisphere in isolation. This view that callosotomy completely isolates the hemispheres has now been revised, in favor of the idea of a dynamic functional reorganization of the two sides of the brain; however, the evidence collected from split-brain patients is still a milestone in the neurosciences. The right-hemispheric superiority found in the healthy population concerning face perception has been further supported with split-brains, and it has been shown that the right disconnected hemisphere appears superior to the left hemisphere in recognizing and processing faces with similar characteristics as the observers’ (e.g., gender, identity, etc.). Even more controversial is the field of hemispheric asymmetries for processing facial emotion, some evidence suggesting a right-hemispheric superiority for all emotions, some others showing a complementary hemispheric asymmetry depending on the positive or negative emotional valence. Although the practice of callosotomy is mostly abandoned today in favor of pharmacological alternatives, further studies on the remaining split-brain patients could help advance our understanding of hemispheric specialization for social stimuli.

What Split-Brain Patients Tell Us about Consciousness

Split-brain patients demonstrate that an intact corpus callosum and, correspondingly, interhemispheric communication are not essential for consciousness. Considering the great abundance of interhemispheric functional connections in the healthy brain (Doron et al., 2012; Salvador et al., 2005), it is surprising that consciousness survives callosotomy, in which nearly all interhemispheric communication is lost. But it does—the two disconnected hemispheres of a split-brain patient appear to possess all of the defining attributes of consciousness (Damasio and Meyer, 2009), such as wakefulness, emotion, attention, and purposeful behavior (Gazzaniga, 2000; LeDoux et al., 1977). However, although consciousness persists after hemispheric disconnection, the conscious experience of split-brain patients may differ from that of healthy individuals since each disconnected hemisphere (especially the right) possesses only a subset of the intact brain’s gamut of cognitive functions.

One possible explanation for the preserved consciousness of split-brain patients is that each hemisphere’s thalamocortical connections remain intact following commissurotomy. Several theories of consciousness, such as the global workspace model (Newman et al., 1997) or dynamic core model (Tononi and Edelman, 1998), posit that consciousness arises through reentrant neural activity of thalamocortical loops (Llinas et al., 1998; Newman et al., 1997; Tononi and Koch, 2008; Tononi, 2004; Ward, 2011). In line with these theories, each hemisphere of a split-brain patient may remain conscious following commissurotomy because the connections between the cortex and thalamus in each hemisphere remain intact. In a related vein, each hemisphere may remain conscious following surgery because of spared cortico-cortical connections. In support of this view, recent fMRI (Monti et al., 2013) and EEG (Boly et al., 2012) studies have shown that loss of consciousness is associated with a decrease in cortico-cortical connectivity, even when thalamocortical connectivity remains unchanged. Spared subcortical and cortico-cortical connections may enable bilateral functional connectivity after split-brain surgery (Uddin et al., 2008). In a recent study, O’Reilly et al. (2013) measured rhesus monkeys’ resting state functional connectivity with fMRI before and after callosotomy. They found that corpus callosum sectioning abolished nearly all interhemispheric functional connectivity, but these effects were mitigated if the anterior commissure was spared. In sum, these theories suggest that both hemispheres of a split-brain patient are conscious because subcortical and intra-hemispheric cortico-cortical connections remain intact following commissurotomy.

Another possible explanation for the preserved consciousness of split-brain patients stems from Giulio Tononi’s integrated information theory (IIT) of consciousness, which posits that consciousness is proportional to the capacity of a system to integrate information, such that greater information integration produces richer conscious experiences (Tononi and Edelman, 1998; Tononi, 2004, 2008; Oizumi et al., 2014). Integrated information, denoted by phi, is determined by a system’s degree of differentiation (a measure of possible conscious experiences) and integration (the degree to which information across modules is unified). According to the theory, the human brain has a large phi—and therefore a rich conscious experience—because it consists of many specialized modules (high differentiation) that can form countless functional assemblies (high integration). The brain’s capacity to integrate information decreases after commissurotomy because interhemispheric connections are lost (less integration) and each hemisphere has fewer specialized modules and possible conscious states than an intact brain (less differentiation). Therefore, according to IIT, the consciousness of each hemisphere should correspondingly decrease. In a computation model of split-brain patients’ capacity for information integration, Tononi (2004) estimates that phi equals 72 in the united brain but only 61 in each disconnected hemisphere. The model predicts that phi decreases after commissurotomy, but not drastically so, because many cognitive functions are present in both cerebral hemispheres. The model is consistent with research on split-brain patients, with one exception: as we have seen, both hemispheres appear to be conscious following commissurotomy, but the conscious experience of the left hemisphere is superior to that of the right. In relation to the integrated information model, these findings may suggest that the disconnected left hemisphere has a greater capacity to integrate information—and therefore a greater phi—than the right hemisphere.

Split-brain patients, in whom the cortical commissures, principally the corpus callosum, have been cut, provide a unique window into functional specialization of each cerebral hemisphere. Early testing of these patients, using various methods for lateralizing stimulus input and responses, confirmed hemispheric specializations suspected from previous studies of patients with lateralized brain damage. The following decades produced many examples of functional differences between the two hemispheres in the attentional, perceptual, and cognitive domains. Comparisons of partial- and complete-callosotomy patients have yielded information about functionally specific pathways through the corpus callosum. Division of the brain has also provided insight into the nature of consciousness in each hemisphere.

VII Corpus Callosum and Consciousness

The study of split-brain patients during the past 40 years has helped change our understanding of the nature of consciousness. It has offered a prime example of the modularization of cognitive processes and documented the distinctions between a dominant and nondominant hemisphere. It has raised the question of whether the callosum may have played a unique role in the development of human consciousness. One of the key observations made regarding the Vogel and Bogen series of commissurotomies was that severing the callosum seemed to yield two separate conscious entities with the ability to respond independently. The idea of a “dual consciousness” was embraced by some scientists such as Pucetti, who hypothesized that the human condition was always made up of dual-consciousnesses that were only revealed after the section of the callosum. Others rejected the status of the right hemisphere as conscious. Daniel Dennett concluded that the right hemisphere had, at best, a “rudimentary self.”

Michael Gazzaniga, Paul Corballis, and Margaret Funnell, recently proposed a new role for the corpus callosum as “the prime enabler for the human condition.” They suggest the corpus callosum allows the brain to be more efficient, allowing hemispheric specialization but permitting integration of specialized functions as needed. In their view, lateral specialization reflects the emergence of new skills and the retention of others. An advantageous mutation that changes the function of one hemisphere can be maintained and flourish while established functions continue without disruption. The callosum permits a reduction of redundant function and the easier acquisition of new skills. They suggest that the corpus callosum facilitated the development of a “theory of mind,” the skills that support the ability to understand the point of view of another creature, by permitting “this extended capacity [to arise] within a limited cortical space.”

The best examples of behavior that appear to represent a separate consciousness in the right hemisphere come from split-brain patients with at least some language capacity. The newest completely split patient with normal intelligence, V.J., is anomalous in that she controls written and spoken output with different hemispheres. She is also unique in another way. She is the first split in my experience who is frequently dismayed by the independent performance of her right and left hands. She is discomforted by the fluent writing of her left hand to unseen stimuli and distressed by the inability of her right hand to write words she can read out loud and spell. In the myriad of articles discussing duality of consciousness, consciousness is sometimes considered as arising from the need for a single serial channel for motor output. In normally lateralized persons, the left hemisphere maintains control of output of both speech and writing. In V.J., there are two centers of control of the motor output of language, one partially disabled but still functional. One problem of this view point is that some split-brain patients, notably J.W. and V.P., also have some control of motor speech from either hemisphere. However, in both of these cases, the control of spoken language developed after the surgical intervention and this sequence of events may have different consequences for the conscious experience of it. If serial control of output is an important determinant of the function experienced as consciousness and the fluent shifting of control of output from one system to another is a part of that function, we may still have a good deal to learn from the split-brain model.

25-6 CONCLUSIONS

Coordinated laterality experiments in split-brain patients and in normal subjects suggest that the disconnected RH underestimates the language competence of the normal RH. The reason is that even when the two normal hemispheres draw on separate lexical representations and exhibit independent strategies, there occur dynamic sharing of resources and variable automatic priming effects across the commissures, which effectively increase RH language competence and range. Even the split brain permits some subcallosal linguistic interhemispheric interaction, including transfer of resources from the disconnected LH to the RH, so that the disconnected RH may overestimate the linguistic competence of the RH following surgical removal or anesthesia of the LH in adulthood.

Lexical variables that show independent effects on word recognition in each normal hemisphere include length (orthographic), concreteness, emotionality, part-of-speech, associative priming, and diverse semantic congruity effects (semantics), derivational morphology (semantic/ phonological), grapheme-phoneme regularity (phonological), and grammatic priming (syntactic).

The new emerging theory from converging clinical and experimental evidence is that RH language competence can assume any of a set of progressive degrees of independence from LH language. With enough resources, the normal RH can even perform grapheme-phoneme correspondence, perhaps also speak. This argues against a strictly modular view of natural language competence. The ability of the normal RH to perform a task then depends not only on its basic competence but also on its concurrent cognitive load, freedom from inhibition, and access to LH resources. Indeed, a similar account may also hold for the normal LH! This is not to argue that RH language competence is as wide as LH competence, but it does suggest greater potential RH competence for online natural language processing than is commonly assumed.

VI. CONCLUSIONS

The study of attention in split-brain patients has been critical to the effort to understand what attentional capacities reside within each of the cerebral hemispheres and how those capacities are integrated. Within this context, the proposal that hemispheric independence depends on whether top-down or bottom-up influences are mediating attentional control has the advantage of being consistent with the putative neural systems involved (see Enns and Kingstone, 1997; Kingstone et al., 1997). The cerebral hemispheres may be labile to independent control via bottom-up influences because these influences presumably derive from subcortical inputs. In this sense, independence may arise when the hemispheres themselves are not directly responsible for deciding how or where to orient attention. Conversely, the hemispheres may compete for attentional control when voluntary or conscious decisions are made regarding what to do with attention, situations where the hemispheres are directly involved in the top-down decision-making process. If so, the idea that the attentional focus is unitary within split-brain patients may only be an illusion of competition for conscious attentional control. Under conditions where both hemispheres are in voluntary agreement as to what to do—for example, performing a visual search task (e.g., Luck et al., 1989, 1994)—then the hemispheres may be equally free to operate independently as they would be under strict bottom-up control.

Abstract

The research studies of complete commissurotomy patients (split-brain) in Roger W. Sperry’s psychobiology laboratory at Caltech, Pasadena, galvanized the scientific and intellectual world in the 1960s and 1970s. The findings had an important and enduring impact on brain research in countless areas. Interest in hemispheric specialization in particular was sparked by these studies and paved the way for countless discoveries. Right hemisphere specialization for visuospatial functions and facial processing was confirmed with these patients. The further unraveling of right-hemisphere cognition, the “mute” hemisphere, was a major goal in Sperry’s laboratory, and much factual knowledge was learned that was not known previously. However, the linking of art and creativity with the right hemisphere was a nonempirically based inference made not by Sperry’s lab but rather by others wishing to “assign” functional hemisphericity. The general assumption was that “art” is anchored in spatial cognition, that it is a nonverbal activity requiring imagery and thus must be controlled by the right, nonlanguage hemisphere. To this day, robust evidence that the right specializes in art expression or art perception is yet to be shown, if for no other reason than that art is not a single, unitary form of expression or cognition. The conjectured right hemisphere–art link turned into a popular story that filtered back into science, shaped future research of brain and art, and overlooked other avenues for insights. This chapter traces and explores this background.

INTRODUCTION

One of several qualities that make split-brain patients so astonishing is that they seem utterly unaware of their special status. The loss of the ability to transfer information from the left hemisphere to the right hemisphere and vice-versa seems to have no impact on their overall psychological state. For example, the sudden loss of the ability to verbally describe the flash of an object to the left visual field seems to be of little concern to them. The truth is that the left brain in these patients does not seem to miss the right brain, despite recent discoveries of several specialized properties in the right hemisphere. That is one of the enduring truths that come out of split-brain research and we believe it has major implications for understanding the physical basis of conscious experience.

In what follows, we argue that consciousness does not constitute a single, generalized process, but that it is an emergent property that arises out of hundreds if not thousands of specialized systems (modules). These systems consist of a neural circuitry specialized to process-specific domains of information [1–3]. These specialized neural circuitries enable the processing and mental representations of a specific aspect of conscious experience, and these circuits are widely distributed throughout the brain. Many of these specialized circuits may be directly connected to some of the other specialized circuits, but not to most of them. Each component competes for attention. From moment to moment, different modules or systems will win and serve as the neural system underlying that moment of conscious experience. Again it is this dynamic, moment-to-moment cacophony of systems that comprises our consciousness. And, yet, we do not experience this as a thousand chattering voices, but as a unified experience. It appears to us as if our consciousness flows easily and naturally from one moment to the next with a single, unified, and coherent narrative. Our sense of a unified experience emerges out of a particular specialized system called the interpreter, which coordinates and continually interprets and makes sense of our behaviours, emotions, and thoughts after they occur. This interpreter appears to be uniquely human and specialized to the left hemisphere.

An important aspect of this view of consciousness is that it is completely dependent on local, specialized components, or modules. If a particular module is impaired or loses its inputs, it alerts the whole system that something is wrong. For example, if the optic nerve is severed, the patient will notice immediately that they are blinded. But if the module itself is removed, as in the case of cortical blindness, then no warning signal is sent and the specific information processed by that specialized system is no longer acknowledged (out of sight, out of mind – so to speak). This creates the peculiar phenomenon that has been observed in a variety of neurological patients that deny that anything is wrong with them despite the clearly observable effects of the brain injury. This aspect of their condition, the unawareness of or denying the existence of their deficit is referred to as anosognosia.

In the next few sections, we will (1) discuss how anosognosia observed in many neurological disorders is indicative of a conscious system that is bound by the inputs of thousands of specialized local modules; (2) review split-brain research, including some recent developments of specialized processes that may contribute to the conscious experience of each hemisphere uniquely; (3) update our understanding of a left hemisphere specialization that we refer to as the ‘interpreter’ that unifies and interprets our conscious experience; and (4) take a speculative look at the world from the point of view of the right hemisphere.

Evidence from Split-Brain Patients

In the 1960s, research by Nobel laureate Roger Sperry and colleagues with split-brain patients dramatically demonstrated the relative specialization of the cerebral hemispheres. In these split-brain patients, the main nerve fiber tract connecting the cerebral hemispheres, the corpus callosum, is severed for the treatment of intractable epilepsy. As a result, higher order information, such as that about an item’s identity (e.g., a car, the letter ‘A,’ and the face of Bill Clinton), cannot be transferred from one hemisphere to the other. Thus, information directed to a single hemisphere is functionally isolated to that hemisphere. This situation provides a unique opportunity to examine the relative specialization of the cerebral hemispheres because each hemisphere’s capabilities can be examined in isolation from those of its partner. As a result, research with split-brain patients has yielded much important information about hemispheric specialization. Absolute differences have been demonstrated only for a couple of functions, namely speech output and phonological processing, which are under sole control of the left hemisphere. Both hemispheres can perform all other tasks, albeit with differing levels of ability and in different manners. Whereas the left hemisphere has a rich ability to perform most all language tasks, the vocabulary of the right hemisphere is much more limited, as is its ability to process complicated grammatical functions. On the other hand, the right hemisphere is superior at processing most types of spatial relationships, especially those involving three-dimensional relations or complicated geometries.

1.05.10.5 The Neocortical Hemispheres and Emotion

Differences between the right and the left hemispheres have mostly been discovered in split-brain patients or in patients with specific lesions of the right or the left hemisphere during presentation of tasks that force the unilateral processing of information (e.g., dichotic listening, fixation). Usually, there is continuous exchange between the hemispheres with the left hemisphere playing an important role in the interpretation and attribution of causes. Lesions of the right hemisphere often lead to emotional indifference or euphoric disinhibition, lesions of the left hemisphere may lead to catastrophic reactions with severe depression. In the interpretation of these results it is important to consider that lesions of one hemisphere may result in a disinhibition and thus overactivation of the other hemisphere. Emotional expression is impaired after lesions in right frontal cortex, emotional recognition and discrimination after right posterior lesions. In right parietal lesions the existence and consequences of disease and/or emotional contents are often denied (sensory and emotional neglect), and emotional expression fades or is inadequate. Electroconvulsive treatment for depression is significantly more effective when applied to the right rather than the left hemisphere. By contrast, a left-sided Wada test leads to a depressed state. For the Wada test a sedative drug is injected in the right or left main brain artery, putting the respective hemisphere to sleep. The sensitivity of the right hemisphere for negative feelings is also supported by the fact that aversive stimuli such as pain or unpleasant odors primarily activate the right and positive stimuli primarily activate the left hemisphere.

In depressive disorders, increased right-frontal activation has been reported, and for mania, increased left-frontal activation. Since motor activity and control of right-handers are regulated predominantly by the left hemisphere, right-hemisphere overactivation leads to difficulty in controlling verbal and motor behaviors. This is supported by the fact that left-handers and ambidextrous persons often show emotional, verbal, and psychosomatic disorders. Dyslexias and allergies as well as hyperactivity and irritable bowel syndrome are more frequent in left-handed persons who have a larger corpus callosum with more fibers and a larger right hemisphere. This has been associated with a larger influence of testosterone during development which facilitates growth of the right hemisphere and inhibits growth of the thymus gland (immune competence) in animal experiments.