The role of Area 10 (BA10) in human multitasking and in social cognition: A lesion study
Highlights
► BA10 is thought to be involved in multitasking and theory of mind (ToM). ► Patients with lesions outside BA10 perform poorly on executive tasks. ► Patients with lesions involving BA10 perform poorly on multitasking and ToM tasks. ► Multitasking abilities are correlated with volume of damage in right lateral BA10. ► Lesions to BA10 produce specific impairments in higher order cognitive functions.
Introduction
The prefrontal cortex (PFC) is the cortical region in the frontal lobe anterior to the primary and association motor cortices. This brain area increases in size with phylogenetic development and, at least in humans, it is thought to be involved in planning complex cognitive behavior and in the expression of personality and appropriate social conduct. The prefrontal cortex is an anatomically and functionally heterogeneous structure and comprises cytoarchitectonically distinct regions, accounting for about 30% of our total cortical area (Fuster, 1997). Understanding the functional organization of the prefrontal cortex and the specific roles played by each of its distinct subregions (e.g. dorsolateral or rostral areas) is an essential issue in human cognitive neuroscience. Large volumes of data derived from functional neuroimaging have led to the statement of multiple influential theories regarding these issues. In order to draw stronger inferences, human lesion studies, which highlight the critical regions within brain networks, are crucial to complement functional neuroimaging approaches.
Brodmann Area 10 (BA10), also known as the frontal pole or rostral/anterior prefrontal cortex, is the largest and most anterior region within the human PFC (Semendeferi, Armstrong, Schleicher, Zilles, & Van Hoesen, 2001). Having experienced remarkable evolutionary expansion, this brain region also shows higher spine density than other areas of the human cortex and is highly interconnected with supramodal areas within the PFC in which information is believed to be represented at its most abstract level (Ramnani & Owen, 2004). All of the above suggests that BA10 plays an important role in human cognition. Accordingly, several authors have placed this brain region at the top of a frontal processing hierarchy (Badre and D’Esposito, 2007, Koechlin et al., 2003).
One function attributed to the anterior PFC is multitasking, in particular, the selection and maintenance of higher order internal goals while other sub-goals are being performed (e.g. Badre and D’Esposito, 2009, Burgess et al., 2007, Gilbert et al., 2005, Gilbert et al., 2006, Gilbert et al., 2007, Koechlin and Summerfield, 2007). Maintenance and flexible retrieval of higher order goals enable us to orient our behavior to internal plans, rather than merely responding to the external environment. Most of the supporting data come from functional neuroimaging studies, and while multitasking and planning deficits have been described in patients with extensive frontal cortex damage (e.g. Goldstein et al., 1993, Hebb and Penfield, 1940, Shallice and Burgess, 1991), there are only a few lesion studies that have systematically assessed the specific role of BA10 in this domain. In a pioneering study, Burgess, Veitch, de Lacy Costello, and Shallice (2000) showed that damage to the more medial and polar aspects of BA8, 9 and 10, in the left hemisphere, was associated with more internal task switching deficits than right dorsolateral prefrontal lesions. However, the specific role of BA10 was not assessed, and the deficits found could also be related to simple rule breaking behavior, which was indeed part of the overall score reported. Recently, Dreher, Koechlin, Tierney, and Grafman (2008) also showed that in a group of patients with frontal lesions, deficits in multitasking correlated with the extent of damage in BA10. However, patients with closed head injuries were included in their study, making it hard to distinguish the effects of focal lesions and more diffuse damage. Two more recent lesion studies (Umeda et al., 2011, Volle et al., 2011) have related rostral prefrontal cortex to prospective memory (the capacity to carry out intended actions after a delayed period of time), perhaps a critical element of multitasking.
Besides the maintenance and retrieval of higher order goals, functional neuroimaging has also linked BA10 to the ability to infer someone else's feelings and thoughts, demanding a complex set of functions collectively referred to as theory of mind. In fact, several functional neuroimaging studies have shown rostral PFC activation when the ability to infer other people's thoughts and emotions was assessed (e.g. Gilbert et al., 2006, Gilbert et al., 2007, Sommer et al., 2007). Again, while some lesion studies have shown that frontal damage can impair performance on theory of mind tasks (Narvid et al., 2009, Rowe et al., 2001, Shamay-Tsoory et al., 2006, Shamay-Tsoory and Aharon-Peretz, 2007, Stone et al., 1998, Stuss et al., 2001), no studies have yet investigated the role of BA10 in particular.
Based on neuroimaging findings, functional specialization within BA10 has been proposed both in the lateral-medial and anterior–posterior axes (Gilbert et al., 2007). Medial BA10, especially its posterior part, is supposed to play a major role in mentalizing and theory of mind (Gilbert et al., 2006, Gilbert et al., 2007). On the other hand, lateral BA10 seems necessary in human multitasking when attending to the outside world is not enough, and an internal goal is needed to direct behavior; that is, when cognition must be directed by stimulus-independent thought (Burgess et al., 2007, Dumontheil et al., 2010, Gilbert et al., 2005, Koechlin and Summerfield, 2007).
In the present study, we examined the role of BA10 both in multitasking and in theory of mind by comparing a group of frontal patients whose lesions affected BA10, a group of frontal patients whose lesions did not affect that area and a group of normal controls. We hypothesized that, if BA10 indeed plays a role in these cognitive functions, patients with lesions affecting this area would have impaired performance on tasks of multitasking and theory of mind relative to controls and patients with nonBA10 lesions. Moreover, given the findings from neuroimaging studies suggesting functional specialization across different BA10 subregions, we examined correlations between behavioral deficits and volume of damage within specific BA10 regions.
Section snippets
Subjects
Fifteen patients with chronic focal frontal lesions were recruited from the Cambridge Cognitive Neuroscience Research Panel at the MRC Cognition and Brain Sciences Unit in Cambridge, UK (n = 11) and from the INECO Research Data Base in Buenos Aires, Argentina (n = 4). All patients had a single focal lesion, verified by MRI, confined to frontal structures. Lesion aetiology was mostly tumor resection or cerebrovascular disease (Table 1). Exclusion criteria were current/previous psychiatric diagnosis,
Results
Mean estimated premorbid IQ was 107.8 (SD = 11.4) for patients without damage in BA10, 117.0 (SD = 10.5) for patients with damage in BA10, and 114.0 (SD = 12.0) for control subjects (see Table 2). Differences between groups in premorbid IQ were not significant (F2,37 = 1.3, p = 0.28). Mean total lesion volume was not significantly different (t12 = 0.74, p = 0.48) between BA10 (56.84 ± 26.94 ml) and nonBA10 (43.33 ± 40.33 ml) patients. Within BA10 patients, no significant differences were found between volumes of
Discussion
In the present study, we examined the role of BA10 in the ability to maintain higher order goals and in theory of mind. We also searched for correlations between task performance and volume of damage across different regions within BA10.
The present investigation shows that prefrontal lesions involving BA10 produce deficits both in theory of mind tasks and in multitasking, while frontal lesions not involving BA10 produced no such deficits. In particular, deficits in multitasking were
Conflict of interest
The authors report no conflicts of interest.
Acknowledgments
This work was supported by the Medical Research Council (intramural program MC_US_A060_0001), and by an International Short Visit award from the Royal Society. FM was funded by a grant from Fundación INECO.
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