Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex

Abstract

Abstract■ Semantic cognition requires a combination of semantic representations and executive control processes to direct activation in a task-and time-appropriate fashion [Jefferies, E., & Lambon Ralph, M. A. Semantic impairment in stroke aphasia versus semantic dementia: A case-series comparison. Brain, 129, 2132Brain, 129, -2147Brain, 129, , 2006. We undertook a formal meta-analysis to investigate which regions within the large-scale semantic network are specifically associated with the executive component of semantic cognition. Previous studies have described in detail the role of left ventral pFC in semantic regulation. We examined 53 studies that contrasted semantic tasks with high > low executive requirements to determine whether cortical regions beyond the left pFC show the same response profile to executive semantic demands. Our findings revealed that right pFC, posterior middle temporal gyrus (pMTG) and dorsal angular gyrus (bordering intraparietal sulcus) were also consistently recruited by executively demanding semantic tasks, demonstrating patterns of activation that were highly similar to the left ventral pFC. These regions overlap with the lesions in aphasic patients who exhibit multimodal semantic impairment because of impaired regulatory control (semantic aphasia)-providing important convergence between functional neuroimaging and neuropsychological studies of semantic cognition. Activation in dorsal angular gyrus and left ventral pFC was consistent across all types of executive semantic manipulation, regardless of whether the task was receptive or expressive, whereas pMTG activation was only observed for manipulation of control demands within receptive tasks. Second, we contrasted executively demanding tasks tapping semantics and phonology. Our findings revealed substantial overlap between the two sets of contrasts within left ventral pFC, suggesting this region underpins domain-general control mechanisms. In contrast, we observed relative specialization for semantic control within pMTG as well as the most ventral aspects of left pFC (BA 47), consistent with our proposal of a distributed network underpinning semantic control. ■

Neural changes associated with semantic processing in healthy aging despite intact behavioral performance

“…It is noteworthy to mention that the peak of the locus of difference of activation in the left posterior middle temporal gyrus found in our study is posterior to the one reported in previous semantic studies in young adults (Noonan, Jefferies, Visser, & Lambon Ralph, 2013). In addition, patterns of cortical activation in older subjects were more widely distributed across both hemispheres than in younger subjects.…”

“…Moreover, Davis et al (2008) and Huang et al (2012) postulated that compensatory neural mechanisms in older adults occur not only in prefrontal regions but also in posterior regions, such as the temporoparietal region, which is less affected by normal aging than prefrontal regions . Along this line, age-related differences may be observed in other cerebral region, such as the posterior middle temporal gyrus, that undertakes the same cognitive process than IPC and might play a more critical role in a comprehensive semantic judgment task (Noonan et al, 2013).…”

“…Although both the IPC and the temporoparietal cortex play a role in selection of context-appropriate and task-oriented semantic knowledge (including the inhibition of inappropriate semantic candidates or distracters), it is not clear at this time whether these two regions play distinct roles within the semantic control system or whether they act synergistically as part of a connected network of regions (Jefferies, 2013). It has been recently proposed that the IPC may be involved in semantic control processing regardless of the receptive/expressive aspects of the task while the posterior temporal middle temporal gyrus may be engaged only when comprehensive task are performed (Noonan et al, 2013). In the current study, age-related changes were found in both of these cortical areas.…”

Early-onset and late-onset Alzheimer's disease are associated with distinct patterns of memory impairment

“…The left posterior middle temporal gyrus has also been identified as an important region of the semantic network (Whitney et al, 2012;Jefferies, 2013;Noonan et al, 2013). More specifically, it has been recently suggested that this region plays a major role in the executive aspects of semantic cognition, including the manipulation and selection of task relevant knowledge as well as the inhibition of task-irrelevant knowledge.…”

Bilingual speech-in-noise: Neural bases of semantic context use in the native language

“…The left angular gyrus is known to play a role in semantic processing (Seghier, Fagan, & Price, 2010), and in executively demanding semantic tasks (Noonan, Jefferies, Visser, & Lambon Ralph, 2013). It has also been found to be implicated in subliminal semantic priming (Diaz & McCarthy, 2007), and in relatedness judgements when word pairs are semantically related compared to when they are unrelated (Chou et al, 2006).…”