Making sense of the world around us depends upon selectively retrieving information relevant to our current goal or context. However, it is unclear whether selective semantic retrieval relies exclusively on general control mechanisms recruited in demanding non-semantic tasks, or instead on systems specialised for the control of meaning. One hypothesis is that the left posterior middle temporal gyrus (pMTG) is important in the controlled retrieval of semantic (not non-semantic) information; however this view remains controversial since a parallel literature links this site to event and relational semantics. In a functional neuroimaging study, we demonstrated that an area of pMTG implicated in semantic control by a recent meta-analysis was activated in a conjunction of (i) semantic association over size judgements and (ii) action over colour feature matching. Under these circumstances the same region showed functional coupling with the inferior frontal gyrus — another crucial site for semantic control. Structural and functional connectivity analyses demonstrated that this site is at the nexus of networks recruited in automatic semantic processing (the default mode network) and executively demanding tasks (the multiple-demand network). Moreover, in both task and task-free contexts, pMTG exhibited functional properties that were more similar to ventral parts of inferior frontal cortex, implicated in controlled semantic retrieval, than more dorsal inferior frontal sulcus, implicated in domain-general control. Finally, the pMTG region was functionally correlated at rest with other regions implicated in control-demanding semantic tasks, including inferior frontal gyrus and intraparietal sulcus. We suggest that pMTG may play a crucial role within a large-scale network that allows the integration of automatic retrieval in the default mode network with executively-demanding goal-oriented cognition, and that this could support our ability to understand actions and non-dominant semantic associations, allowing semantic retrieval to be ‘shaped’ to suit a task or context.
Semantic retrieval involves both (1) automatic spreading activation between highly related concepts and (2) executive control processes that tailor this activation to suit the current context or goals. Two structures in left temporoparietal cortex, angular gyrus (AG) and posterior middle temporal gyrus (pMTG), are thought to be crucial to semantic retrieval and are often recruited together during semantic tasks; however, they show strikingly different patterns of functional connectivity at rest (coupling with the "default mode network" and "frontoparietal control system," respectively). Here, transcranial magnetic stimulation (TMS) was used to establish a causal yet dissociable role for these sites in semantic cognition in human volunteers. TMS to AG disrupted thematic judgments particularly when the link between probe and target was strong (e.g., a picture of an Alsatian with a bone), and impaired the identification of objects at a specific but not a superordinate level (for the verbal label "Alsatian" not "animal"). In contrast, TMS to pMTG disrupted thematic judgments for weak but not strong associations (e.g., a picture of an Alsatian with razor wire), and impaired identity matching for both superordinate and specific-level labels. Thus, stimulation to AG interfered with the automatic retrieval of specific concepts from the semantic store while stimulation of pMTG impaired semantic cognition when there was a requirement to flexibly shape conceptual activation in line with the task requirements. These results demonstrate that AG and pMTG make a dissociable contribution to automatic and controlled aspects of semantic retrieval.
Semantic memory encompasses knowledge of specific objects and their diverse associations, but the mechanisms that allow us to retrieve aspects of knowledge required for a given task are poorly understood. The dual hub theory suggests that separate semantic stores represent knowledge of (i) taxonomic categories (in the anterior temporal lobes, ATL) and (ii) thematic associations (in angular gyrus, AG or posterior middle temporal gyrus, pMTG). Alternatively, the controlled semantic cognition (CSC) framework suggests that semantic processing emerges from the flexible interaction of heteromodal semantic representations in ATL with a semantic control network, which includes pMTG as well as prefrontal regions. According to this view, ATL supports patterns of coherent auto-associative retrieval, while semantic control sites respond when ongoing conceptual activation needs to be altered to suit the task or context. These theories make different predictions about the nature of functional dissociations within the semantic network. We review evidence for these claims across multiple methods. First, we show ATL is sensitive to the strength of thematic associations as well as taxonomic relations. Next, we document functional dissociations between AG and pMTG: rather than these regions acting as comparable thematic hubs, AG is allied to the default mode network and supports more ‘automatic’ retrieval, while pMTG responds when control demands are high. However, the semantic control network, including pMTG, also shows a greater response to events/actions and verbs, supporting the claims of both theories. We propose that tasks tapping event semantics often require greater shaping of conceptual retrieval than comparison tasks, because these elements of our knowledge are inherently flexible, with relevant features depending on the context. In this way, the CSC account might be able to account for findings that suggest both a process and a content distinction within the semantic network. This article is part of the theme issue ‘Towards mechanistic models of meaning composition’.
Semantic cognition, as described by the controlled semantic cognition (CSC) framework (Rogers et al., 2015, Neuropsychologia, 76, 220), involves two key components: activation of coherent, generalizable concepts within a heteromodal 'hub' in combination with modality-specific features (spokes), and a constraining mechanism that manipulates and gates this knowledge to generate time-and task-appropriate behaviour. Executivesemantic goal representations, largely supported by executive regions such as frontal and parietal cortex, are thought to allow the generation of non-dominant aspects of knowledge when these are appropriate for the task or context. Semantic aphasia (SA) patients have executive-semantic deficits, and these are correlated with general executive impairment. If the CSC proposal is correct, patients with executive impairment should not only exhibit impaired semantic cognition, but should also show characteristics that align with those observed in SA. This possibility remains largely untested, as patients selected on the basis that they show executive impairment (i.e., with 'dysexecutive syndrome') have not been extensively tested on tasks tapping semantic control and have not been previously compared with SA cases. We explored conceptual processing in 12 patients showing symptoms consistent with dysexecutive syndrome (DYS) and 24 SA patients, using a range of multimodal semantic assessments which manipulated control demands. Patients with executive impairments, despite not being selected to show semantic impairments, nevertheless showed parallel patterns to SA cases. They showed strong effects of distractor strength, cues and miscues, and probe-target distance, plus minimal effects of word frequency on comprehension (unlike semantic dementia patients with degradation of conceptual knowledge). This supports a component process account of semantic cognition in which retrieval is shaped by control processes, and confirms that deficits in SA patients reflect difficulty controlling semantic retrieval.This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Successful retrieval of semantic knowledge in a context-specific and timely manner depends on the interaction of multiple processes, including (1) the conversion of sensory input into meaning (Sharp, Scott, & Wise, 2004), (2) generalizable conceptual representations (Lambon Ralph, Sage, Jones, & Mayberry, 2010;Patterson, Nestor, & Rogers, 2007), and (3) flexible control over the retrieval of knowledge, such that semantic processing focuses on information appropriate to the context even when this is not necessarily the dominant feature or association ). An interaction between these components is envisaged within the controlled semantic cognition ( , 2010). However, the mechanisms underpinning semantic control are underspecified; in particular, it is unclear the extent to which this capacity draws on domain-gene...
Comprehension deficits are common in both Wernicke’s aphasia and semantic aphasia. Thompson et al. compare these groups of patients on a task in which related items are repeatedly presented, increasing semantic competition across repetitions. Both groups show semantic impairment, but only individuals with prefrontal damage show harmful effects of repetition.
Recent accounts of large-scale cortical organisation suggest that the default mode network (DMN) is positioned at the top of a principal gradient, reflecting the separation between heteromodal and unimodal sensory-motor regions in patterns of connectivity and in geodesic distance along the cortical surface (Margulies et al., 2016). This isolation of DMN from external inputs might allow the integration of disparate sources of information that can constrain subsequent cognition. We tested this hypothesis by manipulating the degree to which semantic decisions for ambiguous words (e.g. jam ) were constrained by preceding visual cues depicting relevant spatial contexts (e.g. supermarket or road ) and/or facial emotions (e.g. happy vs. frustrated ). We contrasted (i) the effects of a single preceding cue with a no-cue condition employing scrambled images, and (ii) convergent spatial and emotion cues with single cues. Single cues elicited stronger activation in the multiple demand network relative to no cues, consistent with the requirement to maintain information in working memory. The availability of two convergent cues elicited stronger activation within DMN regions (bilateral angular gyrus, middle temporal gyrus, medial prefrontal cortex, and posterior cingulate), even though behavioural performance was unchanged by cueing – consequently task difficulty is unlikely to account for the observed differences in brain activation. A regions-of-interest analysis along the unimodal-to-heteromodal principal gradient revealed maximal activation for the convergent cue condition at the heteromodal end, corresponding to the DMN. Our findings are consistent with the view that regions of DMN support states of information integration that constrain ongoing cognition and provide a framework for understanding the location of these effects at the heteromodal end of the principal gradient.
Patients with multimodal semantic impairment following stroke (referred to here as 'semantic aphasia' or SA) fail to show the standard effects of frequency in comprehension tasks. Instead, they show absent or even reverse frequency effects: i.e., better understanding of less common words. In addition, SA is associated with poor regulatory control of semantic processing and executive deficits. We used a synonym judgement task to investigate the possibility that the normal processing advantage for high frequency (HF) words fails to emerge in these patients because HF items place greater demands on executive control. In the first part of this study, SA patients showed better performance on more imageable as opposed to abstract items, but minimal or reverse frequency effects in the same task, and these negative effects of word frequency on comprehension were related to the degree of executive impairment. Ratings from healthy subjects indicated that it was easier to establish potential semantic associations between probe and distracter words for HF trials, suggesting that reverse frequency effects might reflect a failure to suppress spurious associations between HF probes and distracters. In a subsequent experiment, the aphasic patients' performance improved when HF probes and targets were presented alongside low frequency distracters, supporting this hypothesis. An additional study with healthy participants used dual task methodology to examine the impact of divided attention on synonym judgement. Although frequently encountered words were processed more efficiently overall, the secondary task selectively disrupted performance for high but not low frequency trials. Taken together, these results show that positive effects of frequency are counteracted in SA by increases in semantic control requirements for HF words.
Damage to left inferior prefrontal cortex in stroke aphasia is associated with semantic deficits reflecting poor control over conceptual retrieval, as opposed to loss of knowledge. However, little is known about how functional recruitment within the semantic network changes in patients with executive-semantic deficits. The current study acquired functional magnetic resonance imaging (fMRI) data from 14 patients with semantic aphasia, who had difficulty with flexible semantic retrieval following left prefrontal damage, and 16 healthy age-matched controls, allowing us to examine activation and connectivity in the semantic network. We examined neural activity while participants listened to spoken sentences that varied in their levels of lexical ambiguity and during rest. We found group differences in two regions thought to be good candidates for functional compensation: ventral anterior temporal lobe (vATL), which is strongly implicated in comprehension, and posterior middle temporal gyrus (pMTG), which is hypothesized to work together with left inferior prefrontal cortex to support controlled aspects of semantic retrieval. The patients recruited both of these sites more than controls in response to meaningful sentences. Subsequent analysis identified that, in control participants, the recruitment of pMTG to ambiguous sentences was inversely related to functional coupling between pMTG and anterior superior temporal gyrus (aSTG) at rest, while the patients showed the opposite pattern. Moreover, stronger connectivity between pMTG and aSTG in patients was associated with better performance on a test of verbal semantic association, suggesting that this temporal lobe connection supports comprehension in the face of damage to left inferior prefrontal cortex. These results characterize network changes in patients with executive-semantic deficits and converge with studies of healthy participants in providing evidence for a distributed system underpinning semantic control that includes pMTG in addition to left inferior prefrontal cortex.
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