Exploring multimodal semantic control impairments in semantic aphasia: Evidence from naturalistic object use

Abstract

Semantic processing can break down in qualitatively distinct ways in different neuropsychological populations. Previous studies have shown that patients with multimodal semantic impairments following stroke - referred to as semantic aphasia (SA) - show deficits on a range of conceptual tasks due to a failure of semantic control processes in the context of prefrontal and/or temporoparietal infarction. Although a deficit of semantic control would be expected to impair performance in all modalities in parallel, most previous research in this patient group has focussed primarily on tasks employing words. This study explored the consequences of deregulated semantic cognition for an indisputably non-verbal task-naturalistic object use. Patients with SA performed more poorly than control participants on a range of everyday tasks assessed by the Naturalistic Action Test (NAT, Schwartz, M. F., Buxbaum, L. J., Ferraro, M., Veramonti, T., & Segal, M. (2002). Naturalistic action test. Thames Valley Test Company). Moreover, their scores on this assessment correlated with those obtained on language-based semantic tasks, suggesting that a common deficit could underlie the impairment in both modalities. As previously observed in the verbal domain, performance on the NAT was poorer when control processes were taxed by dual-task situations and the inclusion of semantically related distracting objects. A number of characteristics of the patients' action sequences were specifically indicative of deregulated semantic cognition. Their everyday action sequences were highly fragmented by a tendency to abandon subtasks before their completion and engage, instead, in extended periods of aimless "toying" with objects. The patient group also exhibited recurrent perseverative behaviour. These findings parallel the performance of a recurrent connectionist model of naturalistic action developed by Botvinick and Plaut [Botvinick, M. & Plaut, D. C. (2004). Doing without schema hierarchies: A recurrent connectionist approach to normal and impaired routine sequential action. Psychological Review, 111, 395-429], after the mechanism responsible for controlling action in a temporally sensitive manner was damaged. This study provides converging evidence for a failure of control processes underlying semantic memory impairment in SA, which is reflected not only in patients' performance on language-based tasks, but also in the non-verbal domain of naturalistic object use.

Shared neural substrates of apraxia and aphasia

“…These regions form a continuous territory of heteromodal cortex. There is controversy about the precise functions of this large territory and their distribution across its extension but agreement that semantic processing forms part of them (Binder et al, 2009;Simmons and Martin, 2009;Jefferies, 2013;Corbett et al, 2013).…”

What we talk about when we talk about access deficits

“…In particular, performance on these executive function tests has been found to be correlated with lexical-semantic tasks, such as picture naming, word-topicture matching, and picture-picture matching [8,43,46] and action semantic tasks, such as object-directed action knowledge and naturalistic sequential action [43,47]. Importantly, SD patients do not exhibit such correlations between performance on semantic tasks and executive function tests.…”

N-backer: An auditory n-back task with automatic scoring of spoken responses

“…Patients with executive or attentional deficits following brain injury also perform poorly on the same tasks within the NAT, and also show frequent hesitations and toying (Corbett et al, 2009). However, complete action additions and omissions were relatively rare in our healthy participants, and hence there were no striking effects of 2-backing on the diagnostic "NAT score."…”

“…The authors of the NAT explicitly exclude "prolonged struggles to manipulate and use items and misreaching that falls short of taking the object" from the error scores. This misses "toying," a commonly observed behaviour of people with executive impairment following stroke or dementia (e.g., Corbett et al, 2009;Wherton & Monk, 2010), where patients repeatedly touch, move, or aimlessly pick up and then replace an object. This type of directionless and inefficient behaviour was observed when participants were performing 2-back concurrently with the NAT subtasks.…”

“…Sequential object use is thought to be executively demanding (Duncan, Emslie, Williams, Johnson, & Freer, 1996;Giovannetti, Schwartz, & Buxbaum, 2007;Morady & Humphreys, 2009) and is impaired in clinical populations with attentional deficits following stroke or dementia (Corbett, Jefferies, & Lambon Ralph, 2009;Giovannetti et al, 2008;Giovannetti, Schmidt, Sestito, Libon, & Gallo, 2006;Schwartz et al, 1998). Consequently, object use tasks are vulnerable to disruption by demanding secondary tasks (see Giovannetti et al, 2007;Morady & Humphreys, 2009).…”