Getting on the same page: The neural basis for social coordination deficits in behavioral variant frontotemporal degeneration

Abstract

For social interactions to be successful, individuals must establish shared mental representations that allow them to reach a common understanding and “get on the same page”. We refer to this process as social coordination. While examples of social coordination are ubiquitous in daily life, relatively little is known about the neuroanatomic basis of this complex behavior. This is particularly true in a language context, as previous studies have used overly complex paradigms to study this. Although traditional views of language processing and the recent interactive-alignment account of conversation focus on peri-Sylvian regions, our model of social coordination predicts prefrontal involvement. To test this hypothesis, we examine the neural basis of social coordination during conversational exchanges in non-aphasic patients with behavioral variant frontotemporal degeneration (bvFTD). bvFTD patients show impairments in executive function and social comportment due to disease in frontal and anterior temporal regions. To investigate social coordination in bvFTD, we developed a novel language-based task that assesses patients’ ability to convey an object’s description to a conversational partner. Experimental conditions manipulated the amount of information shared by the participant and the conversational partner, and the associated working memory demands. Our results indicate that, although patients did not have difficulty identifying the features of the objects, they did produce descriptions that included insufficient or inappropriate adjectives and thus struggled to communicate effectively. Impaired performance was related to gray matter atrophy particularly in medial prefrontal and orbitofrontal cortices. Our findings suggest an important role for non-language brain areas that belong to a large-scale neurocognitive network for social coordination.

Beyond words: Pragmatic inference in behavioral variant of frontotemporal degeneration

“…One possibility is related to a general limitation in mental flexibility that may be seen on measures or reversal learning. Patients with bvFTD have difficulty on such tasks (Freedman et al, 2013), and this may limit patients from spontaneously generating an alternate interpretation of a scalar implicature containing the word “some.” A second, related, possibility is that bvFTD patients have a social cognitive deficit with perspective-taking and recursive reasoning that interfere with the computation of a scalar implicature (Adenzato et al, 2010; Gregory et al, 2002; Healey et al, 2015; McMillan, Rascovsky, Khella, Clark, & Grossman, 2012; Pardini et al, 2013; Torralva et al, 2007). In the absence of an explicit alternative, the comprehension of the scalar term in Experiment 1 strongly depends upon an individual’s ability to go beyond the linguistic code.…”

Linguistic Aspects of Primary Progressive Aphasia

“…In another condition, patients with bvFTD were asked to describe this scene to a color-blind conversational partner. Despite aural and printed reminders that the partner was color-blind, these patients did not avoid using a color adjective, thus differing from healthy controls (Healey et al 2015). …”

“….’ when describing the location of the moved object. By contrast, the patients with bvFTD did not modify or even use an adjective to clearly designate the moved object, demonstrating their insensitivity to the perspective of a conversational partner (Healey et al 2015). In another condition, patients with bvFTD were asked to describe this scene to a color-blind conversational partner.…”

“…In yet another study (Healey et al 2015), we asked patients with bvFTD to describe to an avatar the movement of a toy from the floor to a bookshelf. The bookshelf contained other toys, some of which overlapped with features of the moved object.…”

“…Regression analyses similarly showed that difficulty with narrative expression is associated in part with right dorsolateral pre-frontal and right anterior temporal GM atrophy (Ash et al 2006). Performance on tasks requiring comprehension of discourse was related to GM atrophy in right frontal regions, including ventral and dorsolateral prefrontal areas (Healey et al 2015, McMillan et al 2013). …”