Frontotemporal lobar degeneration and social behaviour: Dissociation between the knowledge of its consequences and its conceptual meaning

Abstract

Inappropriate social behaviour is an early symptom of frontotemporal lobar degeneration (FTLD) in both behavioural variant frontotemporal dementia (bvFTD) and semantic dementia (SD) subtypes. Knowledge of social behaviour is essential for appropriate social conduct. The superior anterior temporal lobe (ATL) has been identified as one key neural component for the conceptual knowledge of social behaviour, but it is unknown whether this is dissociable from knowledge of the consequences of social behaviour. Here, we used a newly-developed test of knowledge about long-term and short-term consequences of social behaviour to investigate its impairment in patients with FTLD relative to a previously-developed test of social conceptual knowledge. We included 19 healthy elderly control participants and 19 consecutive patients with features of bvFTD or SD and defined dissociations as performance differences between tasks for each patient (Bonferroni-corrected p < .05). Knowledge of long-term consequences was selectively impaired relative to short-term consequences in five patients and the reverse dissociation occurred in one patient. Six patients showed a selective impairment of social concepts relative to long-term consequences with the reverse dissociation occurring in one patient. These results corroborate the hypothesis that knowledge of long-term consequences of social behaviour is dissociable from knowledge of short-term consequences, as well as of social conceptual knowledge. Confirming our hypothesis, we found that patients with more marked grey matter (GM) volume loss in frontopolar relative to right superior ATL regions of interest exhibited poorer knowledge of the long-term consequences of social behaviour relative to the knowledge of its conceptual meaning and vice versa (n = 15). These findings support the hypothesis that frontopolar and ATL regions represent distinct aspects of social knowledge. This suggests that rather than being unable to suppress urges to behave inappropriately, FTLD patients often lose the knowledge of what appropriate social behaviour is and can therefore not be expected to behave accordingly.

The neurophysiological architecture of semantic dementia: spectral dynamic causal modelling of a neurodegenerative proteinopathy

“…Aberrant top-down control may promote inflexible behavioural routines: e.g., food consumption is normally heavily modulated by social mores; where relevant social knowledge is no longer accessible, the imperative to consume available food is likely to lead to faux pas. This interpretation, emphasising a deranged social lexicon rather than a release of frontal controls, is supported by neuropsychological evidence 27 .…”

“…Semantic dementia (SD) is the paradigmatic disorder of the human semantic memory system, characterised by selective, progressive erosion of the meanings of words, sensory objects and concepts [20][21][22][23][24] . Patients typically present with insidious anomic aphasia and loss of vocabulary but as the syndrome evolves, semantic impairment blights all sensory modalities and complex behavioural disturbances supervene, due to impaired understanding and evaluation of socio-emotional signals [25][26][27] . The SD syndrome arises from pathogenic protein deposition; principally targeting one canonical, large-scale connectivity network: the 'semantic appraisal network' .…”

“Looks familiar, but I do not know who she is”: The role of the anterior right temporal lobe in famous face recognition

“…Overall, the typical clinical presentation of right svPPA patients is characterized by behavioral symptoms (e.g., cold interpersonal behavior, loss of empathy) and difficulty with person identification and semantic knowledge for persons (Gorno-Tempini et al, 2004; Snowden et al, 2012; Thompson, Patterson, & Hodges, 2003), with less severe naming deficits and surface dyslexia compared to left svPPA cases (Binney et al, 2016). Consequently, the left temporal lobe has been associated with processing of words and objects (Hodges et al, 1992; Mummery et al, 2000), while the right appears to be associated with processing of socio-emotional stimuli (Rankin et al, 2006; Zahn et al, 2009, 2017). Given the known interplay between handedness and lateralization of domain specific areas (Willems, Peelen, & Hagoort, 2009), the picture is further complicated by the evidence of increased non-right-handedness in svPPA population (Miller et al, 2013).…”

“…Additionally, it has been suggested that the right temporal lobe binds sensory representations recruited for social and emotional processes due to its connections with the limbic system (Oishi et al, 2015; Olson et al, 2007). This would explain the combination of deficits in person identification and impairments in social and behavioral domains observed in patients with damage to the right temporal atrophy, including bvFTD and right variant of svPPA (Kumfor and Piguet, 2012; Rankin et al, 2006; Zahn et al, 2009, 2017). Recognizing a face as familiar has cognitive implications (promoting retrieval of person-specific information), as well as behavioral ramification (allowing selection of the appropriate course of action) and emotional consequences (impacting social interaction and personal feelings).Therefore, a second line of research would investigate possible correlations between patients’ performance in familiarity judgment tasks and measures of social cognition, such as emotional face comprehension (Rosen et al, 2002).…”

Neurocognitive measures of self-blame and risk prediction models of recurrence in major depressive disorder

“…It is notable that the original formulations of the “Default Mode Network” based on positron emission tomography included the superior ATL(32). Our focus on the right superior ATL is based on its predominance for socio-emotional functions(30, 33) (22, 30, 34-36) relative to the left ATL. This concords with the efficacy of right temporal electroconvulsive therapy in MDD(37), response to which was predicted by right ATL-frontal connectivity including the SCC(38).…”