Social cognition in patients following surgery to the prefrontal cortex

https://doi.org/10.1016/j.pscychresns.2014.08.007Get rights and content

Highlights

  • We measured social cognition in patients with discrete prefrontal lesions.

  • Patients with ventromedial lesions were impaired in Theory of Mind.

  • The ventromedial group were impaired at recognising emotional faces.

  • The ventromedial prefrontal cortex has functionally heterogeneous subregions.

  • We propose a neuroanatomical model of social cognition.

Abstract

Impaired social cognition, including emotion recognition, may explain dysfunctional emotional and social behaviour in patients with lesions to the ventromedial prefrontal cortex (VMPFC). However, the VMPFC is a large, poorly defined area that can be sub-divided into orbital and medial sectors. We sought to investigate social cognition in patients with discrete, surgically circumscribed prefrontal lesions. Twenty-seven patients between 1 and 12 months post-neurosurgery were divided into groups based on Brodmann areas resected, determined by post-surgical magnetic resonance imaging. We hypothesised that patients with lesions to the VMPFC (n=5), anterior cingulate cortex (n=4), orbitofrontal cortex (n=7) and dorsolateral prefrontal cortex (DLPFC, n=11) would perform worse than a control group of 26 extra-cerebral neurosurgery patients on measures of dynamic facial emotion recognition, theory of mind (ToM) and empathy. Results indicated the VMPFC-lesioned group performed significantly worse than the control group on the facial emotion recognition task overall, and for fear specifically, and performed worse on the ToM measure. The DLPFC group also performed worse on the ToM and empathy measures, but DLPFC lesion location was not a predictor of performance in hierarchical multiple regressions that accounted for other variables, including the reduced estimated verbal IQ in this group. It was concluded that isolated orbital or medial prefrontal lesions are not sufficient to produce impairments in social cognition. This is the first study to demonstrate that it is the combination of lesions to both areas that affect social cognition, irrespective of lesion volume. While group sizes were similar to other comparable studies that included patients with discrete, surgically circumscribed lesions to the prefrontal cortex, future large, multi-site studies are needed to collect larger samples and confirm these results.

Introduction

Patients with lesions to the ventromedial (VM) prefrontal cortex (PFC) display a specific syndrome of behavioural disturbances, including severe changes in emotional and social function that some researchers have suggested are related to poor recognition of emotion (Hornak et al., 2003, Mah et al., 2004). These patients often exhibit disinhibited behaviour, are socially inappropriate, are impulsive, have poor judgment and decision-making, have blunted emotional experience, have difficulty monitoring themselves, and lack awareness of their behaviour (Eslinger and Damasio, 1985, Barrash et al., 2000, Beer et al., 2006). Thus, patients with VMPFC lesions have been likened to sociopaths (Eslinger and Damasio, 1985, Blair and Cipolotti, 2000). Lesions to this area can lead to severely negative psychosocial consequences, including loss of employment, divorce and bankruptcy (Eslinger and Damasio, 1985).

A difficulty with research in these patients is that organic lesions are not selective, and those affecting the VMPFC are often large and involve parts of the orbital (OFC) and medial (MPFC) PFC, both of which have been separately implicated in emotion recognition and social cognition. For example, OFC lesions result in impairments in recognition of facial and vocal emotional expressions (Hornak et al., 2003), and other nonverbal social and emotional cues such as body language (Mah et al., 2004). Lesions to the MPFC also result in impaired recognition of facial and vocal emotion (Hornak et al., 2003, Baird et al., 2006). Neuroimaging studies have observed activation in a part of the MPFC known as the anterior cingulate cortex (ACC) in response to a range of emotional facial expressions (George et al., 1993, Dolan et al., 1996, Morris et al., 1998, Phillips et al., 1998, Blair et al., 1999, Wicker et al., 2003), particularly sadness (Phan et al., 2004). Another potential explanation for impaired social behaviour in patients with VMPFC lesions is that they have deficits in empathy, an ability to share the emotions of others (Singer, 2006), that is disrupted in patients with OFC lesions (Grattan et al., 1994, Eslinger, 1998, Shamay-Tsoory et al., 2003, Shamay-Tsoory et al., 2005, Hynes et al., 2006). Also a key factor for social interactions is the understanding of the thoughts and intentions of others, which includes theory of mind (ToM) (Premack and Woodruff, 1978) or mentalizing (Frith and Frith, 1999), functions that have been demonstrated in neuroimaging studies to involve the MPFC (Frith and Frith, 1999, Gallagher and Frith, 2003).

Thus, subcomponents of the VMPFC may offer distinct contributions to social cognition. While many studies poorly define the VMPFC, a noteworthy exception is the study by Hornak et al. (2003) which investigated recognition of emotion in patients with surgically circumscribed lesions to the PFC. Such an approach had the advantage of determining more precisely the role of subcomponents of the PFC in emotion recognition. The present study adopted this approach and furthered the earlier work in a number of ways, including by dynamically varying the intensity of expression in the facial emotion recognition task and by measuring social cognition in the form of ToM and empathy. The present study also included more precise radiological analysis of post-surgical magnetic resonance imaging (MRI) scans to allow a finer classification of patients into groups based on Brodmann areas (BAs) resected. To reduce the potential influence of compensatory recovery mechanisms, we used strict inclusion criteria of patients between 1 and 12 months post-surgery. Finally, an additional improvement was the inclusion of a non-cerebral neurosurgical control group.

Given that the OFC and MPFC have both been implicated in the recognition of facial emotion, it was hypothesised that these two groups and the VM group would be impaired on a test of dynamic facial emotion recognition compared with a control group of extra-cerebral neurosurgery patients. It was also hypothesised that patients with MFPC lesions would be impaired on a ToM measure, that patients with OFC lesions would be impaired on an empathy measure, and that patients with VMPFC lesions would be impaired on both measures. Finally, based on a study using a reward-related task (Hornak et al., 2004), it was hypothesised that any impairment in social cognition in a group with dorsolateral PFC (DLPFC) lesions would be related to impairments in attention.

Section snippets

Participants

Participants were 27 patients post-neurosurgery to the PFC, with a single surgical resection cavity confirmed by MRI. Of these, 25 were recruited from a neurosurgical inpatient ward and outpatient neurosurgery clinic at the Royal Melbourne Hospital. Two patients were recruited from an inpatient ward of St Vincent׳s Hospital, Melbourne. Control participants were 26 patients post-spinal surgery at the Royal Melbourne Hospital, who had undergone cervical and lumbar laminectomy, discectomy or

Screening measures

Table 3 shows no significant group differences on the FAST or Picture Completion test. There was, however, a significant effect of group for WRAT-R standard score.

Post-hoc tests found the ACC and the DL groups had a significantly lower estimated IQ than the control group, p<0.05. A Kruskal–Wallis test found a significant difference between groups in TEA score. Follow-up Mann–Whitney tests found that both the ACC (p<0.05) and VM (p<0.001) groups scored significantly lower than the control group.

Discussion

We investigated social cognition in patients with discrete surgical lesions to the prefrontal cortex including the ACC, OFC, VMPFC and DLPFC. This study is noteworthy for its attempted methodological improvements upon previous research. Our radiological measurement using post-surgical structural MRI sets the present study apart from existing lesion work in this area, allowing more confident inferences regarding specific functional roles of these sectors. Limiting the inclusion criteria from up

Acknowledgements

The authors thank the participants of this study and also Scott Langenecker and Jon-Kar Zubieta for their comments on an earlier draft.

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