Study Guide: Brain Connectivity and the Self: The Case of Cerebral Disconnection

Recent years have seen a surge of interest in the study of self-related cognition among psychologists and cognitive neuroscientists. Concurrently, lesion and neuroimaging studies have highlighted the necessity of intact cortico-cortical and cortico-subcortical connections for supporting high-level cognitive functions. "Split-brain" patients, who have undergone commissurotomy—a surgical procedure involving the severing of the corpus callosum—provide invaluable insights into the role of these cerebral commissures in sustaining an individual’s sense of self. These patients reveal distinct self-representation capabilities in each hemisphere, giving researchers a unique opportunity to study the lateralization of cognitive functions. This review synthesizes empirical research concerning self-related processes in patients with various disconnection syndromes, focusing particularly on studies investigating self-recognition, ownership, and agency. Collectively, this body of work suggests that a functional corpus callosum, which facilitates interhemispheric transfer, is essential for certain types of self-representations, especially those connected to a cohesive sense of identity and agency.

The concept of the self is a major subject in psychology and neuroscience yet encompasses various cognitive phenomena, making it challenging to define precisely. As noted by Klein & Gangi (2010), there is a lack of a universally accepted definition of the self; nonetheless, it is understood that the self arises from specific brain states and processes. A valuable distinction can be made between the physical and psychological aspects of the self: the physical aspects are typically studied in the context of self-face recognition, agency, and perspective taking, while psychological aspects are investigated through self-knowledge and autobiographical memory studies (Gillihan & Farah, 2005). Neuroimaging studies have consistently shown that physical and psychological self-related processes engage distinct large-scale brain networks connected to various regions including the prefrontal cortex, temporal lobes, and parietal lobes (Lieberman, 2007; Uddin et al., 2007). The ongoing quest among researchers is to identify the precise brain states and processes that underlie various forms of self-representation, while exploring their interactions, which has yielded mixed findings. Ultimately, self-representation, like other complex cognitive functions, likely depends upon the integrity and robust communication within large-scale brain networks (Bressler & Menon, 2010).

Commissurotomy has been recognized as a highly effective treatment for minimizing the spread of epileptic seizures (Bogen & Vogel, 1976; Gazzaniga et al., 1962). This surgical intervention, while used less frequently due to the availability of more effective pharmacological treatments, remains necessary in several cases of intractable epilepsy. Behavioral testing of split-brain patients has provided significant insights into the specialized functions of each cerebral hemisphere and has contributed to a deeper understanding of the corpus callosum's pivotal role in human cognition (Zaidel & Clarke, 1990; Gazzaniga, 2005). Moreover, callosal abnormalities may arise not only from surgical interventions but also from congenital conditions, such as agenesis of the corpus callosum, or can be caused by acquired brain injuries, tumors, or cerebrovascular accidents.

This review seeks to summarize the current understanding regarding self-representation in split-brain patients and others with lesions impacting the cerebral commissures, concentrating particularly on visual self-face recognition and agency—the sense of ownership regarding one’s actions. The test of self-recognition serves as a common experimental method for assessing self-awareness. Early developmental research by Preyer (1889) established the significance of self-concept and its trajectory through observations of children’s behaviors towards their reflections. Amsterdam (1972) found compelling evidence that children demonstrate self-recognition in mirror tests as early as two years of age, coinciding with their nascent use of personal pronouns. Furthermore, Gallup's pioneering research suggested that the ability to recognize oneself in a mirror is deeply intertwined with a fundamental self-concept (Gallup, 1977).

Recent functional magnetic resonance imaging (fMRI) studies have illuminated that, in intact adult brains, the process of self-face recognition activates a fronto-parietal network predominantly located in the right hemisphere, which is integral to self-referential thought processes (Platek et al., 2006; Sugiura et al., 2005; Uddin et al., 2005a). In investigating split-brain patients, Preilowski implemented a scleral contact lens system that allowed one hemisphere to view stimuli at a time, yielding revealing outcomes. Both split-brain patients demonstrated heightened skin resistance—an arousal index—when viewing their own faces, a finding that persisted even when stimuli could not be verbally articulated. This led Preilowski to conjecture the existence of conscious awareness in both hemispheres (Preilowski, 1977).

In addition, Sperry et al. (1979) tested the reactions of split-brain patients to familiar and personally significant stimuli, concluding that both hemispheres could indeed develop a self-concept. When tasked with identifying their own photo among similar images, patients exhibited comparable recognition abilities across hemispheres, thereby negating the notion of lateralized self-awareness. Further studies employing morphed face stimuli revealed differential biases in recognition; while the right hemisphere exhibited a tendency to recognize morphed images as belonging to familiar others, the left hemisphere tended to identify them as self. This may imply that, contrary to the belief that both hemispheres are equally capable of self-recognition, the left hemisphere might have a less stringent criterion for self-representation (Turk et al., 2002).

Keenan and colleagues reinforced these findings by evaluating a callosotomy patient with morphed self-face stimuli, differentiating response modalities correlated to hemispheric processing. Results indicated an enhanced sensitivity to self-recognition in the right hemisphere, although the reliability of using response hand as an indicative factor in hemispheric performance was subsequently questioned (Weems & Zaidel, 2005).

Alien hand syndrome (AHS) offers a remarkable illustration of the challenges associated with establishing a cohesive sense of self. Patients suffering from AHS deny ownership of one hand, or their hand engages in involuntary movements that contradict the actions of the other. Initial discussions surrounding AHS distinguished between frontal AHS—linked with reflexive grasping—and callosal AHS, which is characterized by intermanual conflict (Brion & Jedynak, 1972; Feinberg et al., 1992). Aboitiz and colleagues classified AHS into four categories: (1) diagnostic dyspraxia/intermanual conflict; (2) alien hand sign; (3) anarchic hand; and (4) supernumerary hands (Aboitiz et al., 2003).

The varying mechanisms underlying AHS underscore the critical role of the corpus callosum in maintaining an integrated self-perception concerning body awareness and action planning. Integrity of the anterior corpus callosum is necessary for awareness related to the initiation of goal-directed movements, while the posterior corpus callosum plays a pivotal role in perceptions of limb ownership. Hence, unlike self-face recognition, feelings of ownership over one’s actions and body necessitate interhemispheric communication, facilitated by the corpus callosum.

Research involving individuals with corpus callosum lesions presents a nuanced narrative regarding self-representations in the brain.Self-face recognition appears accessible to both hemispheres independently and does not necessitate interhemispheric communication. Conversely, subjective feelings of limb ownership and agency are dependent on the integrity of both the anterior and posterior corpus callosum, as well as functional connections involving fronto-parietal systems. Bogen’s initial observations revealed that patients exhibited minimal functional impairments in routine behaviors following split-brain surgery (Bogen et al., 1965). This remarkable adaptation raises intriguing speculation that some information may continue to transfer between hemispheres via subcortical routes, even in the absence of cortical commissures (Funnell et al., 2000). Recently, findings utilizing functional MRI in a complete commissurotomy patient indicate that low-frequency BOLD signals reveal residual functional connectivity between disconnected hemispheres, suggesting viable subcortical coordination of cortical networks (Uddin et al., 2008).

Future research should consider additional dimensions of self-related cognition in split-brain patients. While substantial emphasis has been placed on the physical dimensions of the self, exploring psychological factors such as autobiographical memory and self-knowledge are critical for elucidating the corpus callosum’s role in sustaining the psychological self. Split-brain patients provide an extraordinary case study that highlights the complex and multifaceted nature of the self, challenging the notion of a cohesive identity as articulated by Sherrington (1941) and suggesting that various dimensions of the self are governed by distributed neural systems.