Social cognitive deficits and their neural correlates in progressive supranuclear palsy

Abstract

Although progressive supranuclear palsy is defined by its akinetic rigidity, vertical supranuclear gaze palsy and falls, cognitive impairments are an important determinant of patients' and carers' quality of life. Here, we investigate whether there is a broad deficit of modality-independent social cognition in progressive supranuclear palsy and explore the neural correlates for these. We recruited 23 patients with progressive supranuclear palsy (using clinical diagnostic criteria, nine with subsequent pathological confirmation) and 22 age- and education-matched controls. Participants performed an auditory (voice) emotion recognition test, and a visual and auditory theory of mind test. Twenty-two patients and 20 controls underwent structural magnetic resonance imaging to analyse neural correlates of social cognition deficits using voxel-based morphometry. Patients were impaired on the voice emotion recognition and theory of mind tests but not auditory and visual control conditions. Grey matter atrophy in patients correlated with both voice emotion recognition and theory of mind deficits in the right inferior frontal gyrus, a region associated with prosodic auditory emotion recognition. Theory of mind deficits also correlated with atrophy of the anterior rostral medial frontal cortex, a region associated with theory of mind in health. We conclude that patients with progressive supranuclear palsy have a multimodal deficit in social cognition. This deficit is due, in part, to progressive atrophy in a network of frontal cortical regions linked to the integration of socially relevant stimuli and interpretation of their social meaning. This impairment of social cognition is important to consider for those managing and caring for patients with progressive supranuclear palsy.

Figure 1

Voice emotion recognition test, shown separately for each emotion. Progressive supranuclear palsy deficits are seen in a wide range of emotions. Controls are shown in light grey and patients in black. Significance is indicated by asterisks. **Significant difference using Bonferroni correction for seven tests (P < 0.007); and ***P < 0.001. Error bars show standard error.

Figure 2

Theory of mind on TASIT test. Sincere, sarcastic and paradoxical sarcasm categories from TASIT test. Controls are shown in light grey and patients in black. Using Bonferroni correction for three tests, ** indicates a significant result (P < 0.01); *** P < 0.001. Error bars show standard error.

Figure 3

SPM(t) of atrophy in grey (A) and white (B) matter in patients with progressive supranuclear palsy versus controls (threshold P < 0.001 uncorrected, overlaid on representative T₁ brain in standard space using the MNI template).

Figure 4

SPM(t) map of atrophy in grey (A) and white (B) matter seen in patients with progressive supranuclear palsy when regressed with voice emotion scores. Illustrated at P < 0.001 uncorrected.

Figure 5

SPM(t) map of atrophy in grey (A) and white (B) matter that correlates negatively with TASIT scores. Illustrated uncorrected for multiple comparisons, threshold of P < 0.001 (Tables 5 and 6).