Humour processing in frontotemporal lobar degeneration: A behavioural and neuroanatomical analysis

Abstract

Humour is a complex cognitive and emotional construct that is vulnerable in neurodegenerative diseases, notably the frontotemporal lobar degenerations. However, humour processing in these diseases has been little studied. Here we assessed humour processing in patients with behavioural variant frontotemporal dementia (n = 22, mean age 67 years, four female) and semantic dementia (n = 11, mean age 67 years, five female) relative to healthy individuals (n = 21, mean age 66 years, 11 female), using a joint cognitive and neuroanatomical approach. We created a novel neuropsychological test requiring a decision about the humorous intent of nonverbal cartoons, in which we manipulated orthogonally humour content and familiarity of depicted scenarios. Structural neuroanatomical correlates of humour detection were assessed using voxel-based morphometry. Assessing performance in a signal detection framework and after adjusting for standard measures of cognitive function, both patient groups showed impaired accuracy of humour detection in familiar and novel scenarios relative to healthy older controls (p < .001). Patient groups showed similar overall performance profiles; however the behavioural variant frontotemporal dementia group alone showed a significant advantage for detection of humour in familiar relative to novel scenarios (p = .045), suggesting that the behavioural variant syndrome may lead to particular difficulty decoding novel situations for humour, while semantic dementia produces a more general deficit of humour detection that extends to stock comedic situations. Humour detection accuracy was associated with grey matter volume in a distributed network including temporo-parietal junctional and anterior superior temporal cortices, with predominantly left-sided correlates of processing humour in familiar scenarios and right-sided correlates of processing novel humour. The findings quantify deficits of core cognitive operations underpinning humour processing in frontotemporal lobar degenerations and suggest a candidate brain substrate in cortical hub regions processing incongruity and semantic associations. Humour is a promising candidate tool with which to assess complex social signal processing in neurodegenerative disease.

Pathological Joking or Witzelsucht Revisited

“…Dementias, particularly if frontally-predominant, can increase the production of humor, as well as decrease the sense of humor. In particular, patients with bvFTD, especially if right predominant, may have a tendency to Witzelsucht, moria, slapstick, scatological jokes or compulsive punning, along with decreased comprehension of complex or unfamiliar humor {8, 9, 15}. There are also developmental or genetic causes for pathological humor, such as Angelman or the “happy puppet’ syndrome, Williams syndrome, and Down’s syndrome.…”

“…It is likely that both left and right frontal lobes have a role in incongruity detection and incongruity resolution, with the left frontal lobe more responsive to simple humor and the right engaged with more externally-generated, complex humor {30, 34}. Simple humor engages the left frontal lobe [the inferior frontal gyri (IFG)], with input from the medial temporal gyri (MTG) {11,15, 32, 36}. Examples of “simple humor” include the early detection of basic norm violations and plausibility, physical humor, slapstick, puns, familiar humor, and congruent but unfunny endings.…”

“…They may not appreciate the relationship of their punchlines to their storylines and do not experience their funniness, prefering non-funny endings {10, 11, 43–45}. Hence, patients with right frontal lesions, like those with bvFTD {15}, are prone to simple, silly jokes {46}. These findings suggest that damage to the right dorsolateral/ventrolateral frontal lobe, possibly SFG but also MFG and IFG, impairs the integration of externally-generated humor so that it can be experienced as funny {35, 36, 45, 47}.…”

Prosocial deficits in behavioral variant frontotemporal dementia relate to reward network atrophy

“…Behavioral variant frontotemporal dementia (bvFTD) is a neurodegenerative disease that is characterized by a gradual deterioration of social behavior and empathy (Baez et al., 2014; Clark et al., 2015; Gleichgerrcht, Torralva, Roca, Pose, & Manes, 2011; Hsieh, Hornberger, Piguet, & Hodges, 2012). In bvFTD, atrophy in emotion‐ and reward‐relevant neural systems may alter patients’ responsivity to affective cues, thereby impairing their ability to share, intuit, and respond to the needs of others (Henry, Phillips, & von Hippel, 2014; Rankin et al., 2006; Snowden et al., 2008).…”

“…Although previous studies have determined that patients with bvFTD lack empathy, perspective‐taking, insight, and social understanding (Clark et al., 2015; Kumfor & Piguet, 2012; Rosen et al., 2014; Shany‐Ur et al., 2014; Snowden et al., 2008), relatively little is known about how prosociality deteriorates in bvFTD. Recent studies have shown that despite intact perceptions of fairness and basic bargaining skills, patients with bvFTD are unable to use socially relevant contextual information and, therefore, tend to make decisions that benefit themselves over others (Ibanez et al., 2016, 2017; Melloni et al., 2016; O'Callaghan & Hornberger, 2017; O'Callaghan et al., 2016).…”