The relationship between affective decision-making and theory of mind in the frontal variant of fronto-temporal dementia
Introduction
The frontal variant of fronto-temporal dementia (fvFTD) is a prevalent form of early onset dementia with limited techniques available for detection and treatment (Ratnavalli, Brayne, Dawson, & Hodges, 2002). Patients with fvFTD present with profound changes in aspects of social cognition that are present from early in the illness course. Common behavioural symptoms include impulsivity and socially inappropriate behaviour, lack of empathy for others, lack of insight, and impaired decision-making in daily activities. Many of these features are also seen in patients with damage to the orbital aspect of the prefrontal cortex (Damasio, 1994; Malloy, Bihrle, Duffy, & Cimino, 1993) and recent brain imaging data indicate consistent anatomical and functional abnormalities in the orbito-frontal cortex (OFC) in fvFTD patients (Diehl et al., 2004, Ibach et al., 2004, Salmon et al., 2003).
Two capacities that are critical for healthy social behaviour, theory of mind (TOM; the capacity to infer the likely thoughts and intentions of others) and decision-making, are characteristically impaired in fvFTD (Gregory et al., 2002; Lough & Hodges, 2002; Lough et al., 2006). In a similar vein, patients with orbito-frontal lesions are also bad at ToM tasks including detection of deception (Stuss, Gallup, & Alexander, 2001), faux pas (Stone, Baron-Cohen, & Knight, 1998) and cheating (Stone, Cosmides, Tooby, Kroll, & Knight, 2002). Both groups appear to lack empathy (Lough et al., 2006; Rankin, Kramer, & Miller, 2005; Shamay-Tsoory, Tomer, Berger, & Aharon-Peretz, 2003).
Decision-making associated with differing probabilities of reward and punishment has been termed ‘affective’ decision-making. In fvFTD, Rahman and co-workers (Rahman, Sahakian, Hodges, Rogers, and Robbins (1999) demonstrated abnormal betting behaviour using the Cambridge gambling task in patients with fvFTD compared to age-matched controls. In the Iowa gambling task (IGT), a classic test of decision-making ability, OFC lesion patients persist in making choices associated with high immediate rewards but greater long-term punishments (Bechara, Damasio, Damasio, & Anderson, 1994). Their performance has been explained on the basis of impaired somatic markers as an ‘insensitivity to future rewards’ (Bechara, Damasio, & Damasio, 2000). Briefly, the somatic marker hypothesis suggests that bodily states (somatic markers), induced by emotions, come to be associated with positive or negative outcomes, and in turn influence future decision-making by reinvoking the state via the somatosensory cortex (Damasio, 1996). This is believed to increase the efficiency of decision-making by biasing the individual (overtly or covertly) toward particular outcomes.
Thus both ToM and decision-making are linked to the integrity of the orbito-frontal cortex (Bechara et al., 1994; Berthoz, Armony, Blair, & Dolan, 2002; Gregory et al., 2002; Sabbagh, Moulson, & Harkness, 2004; Stone et al., 1998). Since this region is believed to be one of the earliest sites of pathology in fvFTD (Kril & Halliday, 2004), sensitive neuropsychological measures of affective decision-making and social cognition could have clinical utility in the early detection of cognitive dysfunction in fvFTD patients.
From a neuropsychological, and indeed, anatomical perspective, the relationship between the theory of mind and decision-making remains unclear. Successful performance on the Iowa gambling task does not seem to place any demands on the ability to infer others’ beliefs and intentions. Conversely, even difficult ToM tasks may load only negligibly on decision-making systems. Nonetheless, the prefrontal mechanisms of these sets of processes appear to overlap (Bechara et al., 1994, Berthoz et al., 2002, Gregory et al., 2002, Sabbagh et al., 2004, Stone et al., 1998). One possibility is that the spatial resolution of group lesion studies is insufficient to detect anatomical dissociations between decision-making and ToM processes within the orbito-frontal region, an area of the brain with documented functional heterogeneity (O’Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001; Ongur, Ferry, & Price, 2003). Another explanation is that the extended neural circuitry involved in decision-making and ToM are distinct, and the orbito-frontal cortex simply represents the one area of convergence in two independent circuits. A further possibility is that a higher-order mechanism may regulate both affective decision-making and ToM via a common resource (Adolphs, 2003).
There were two main objectives in the present study. The first was to investigate the sensitivity of the Iowa gambling task in patients with early/mild stages of fvFTD, which has not been done previously. The second objective was to examine the relationship between deficits in affective decision-making and ToM in the same group of patients with frontal lobe degeneration. We hypothesized that performance on the decision-making and theory of mind tasks would correlate based on a shared neural substrate in the orbito-frontal cortex.
Section snippets
Subjects
Twenty fvFTD patients were recruited as part of a broader ongoing study on fronto-temporal dementia currently being conducted at the Cognitive Neurology Division Raul Carrea Institute for Neurological Research. The present study only included patients with early/mild stages of fvFTD. All presented with prominent changes in personality plus social behaviour verified by a caregiver. They showed frontal atrophy on MRI or hypoperfusion on SPECT and there were variable deficits on tests of frontal
Background neuropsychological performance and MRI data
Table 1 summarizes demographic and neuropsychological performance for fvFTD, and control groups. The groups were well matched for age (t28 = 1.3, P = 0.2), gender (Fisher exact test, P = 0.70) and education level (U = 97.5, P = 0.9).
fvFTD patients had lower scores than controls for the MMSE (t28 = 2.9, P = 0.007) and the ACE (t28 = 2.7, P = 0.01). Measures of attention and processing speed showed no difference between groups on forward digit span, but trails A performance by fvFTD patients was worse than
Discussion
This study is, to the best of our knowledge, the first to examine the Iowa gambling task in patients with fvFTD, and to combine measures of ToM and decision-making in this group. We found the Iowa gambling task to be particularly sensitive to cognitive dysfunction in patients with early/mild fvFTD. There was another important finding: performance on ToM and decision-making tasks showed no association in fvFTD, while scores on the two ToM tasks were closely correlated.
Acknowledgements
This research was supported in part by a grant from the Raul Carrea Institute for Neurological Research, Buenos Aires, Argentina. Dr. C. Kipps is supported by the Wellcome Trust (Grant no.: 073580), and Prof. J. Hodges is supported by the UK-MRC (Programme Grant). The authors thank Agustina Lacroze for help in testing patients and controls.
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Present address: Institute of Cognitive Neurology (INECO), Castex 3293 (1425), Buenos Aires, Argentina.