Glyn Hallam

Exploring the role of the posterior middle temporal gyrus in semantic cognition : Integration of anterior temporal lobe with executive processes

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.

Representing Representation: Integration between the Temporal Lobe and the Posterior Cingulate Influences the Content and Form of Spontaneous Thought.

When not engaged in the moment, we often spontaneously represent people, places and events that are not present in the environment. Although this capacity has been linked to the default mode network (DMN), it remains unclear how interactions between the nodes of this network give rise to particular mental experiences during spontaneous thought. One hypothesis is that the core of the DMN integrates information from medial and lateral temporal lobe memory systems, which represent different aspects of knowledge. Individual differences in the connectivity between temporal lobe regions and the default mode network core would then predict differences in the content and form of people’s spontaneous thoughts. This study tested this hypothesis by examining the relationship between seed-based functional connectivity and the contents of spontaneous thought recorded in a laboratory study several days later. Variations in connectivity from both medial and lateral temporal lobe regions was associated with different patterns of spontaneous thought and these effects converged on an overlapping region in the posterior cingulate cortex. We propose that the posterior core of the DMN acts as a representational hub that integrates information represented in medial and lateral temporal lobe and this process is important in determining the content and form of spontaneous thought.

Automatic and Controlled Semantic Retrieval: TMS Reveals Distinct Contributions of Posterior Middle Temporal Gyrus and Angular Gyrus

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. SIGNIFICANCE STATEMENT We demonstrate a novel functional dissociation between the angular gyrus (AG) and posterior middle temporal gyrus (pMTG) in conceptual processing. These sites are often coactivated during neuroimaging studies using semantic tasks, but their individual contributions are unclear. Using transcranial magnetic stimulation and tasks designed to assess different aspects of semantics (item identity and thematic matching), we tested two alternative theoretical accounts. Neither site showed the pattern expected for a “thematic hub” (i.e., a site storing associations between concepts) since stimulation disrupted both tasks. Instead, the data indicated that pMTG contributes to the controlled retrieval of conceptual knowledge, while AG is critical for the efficient automatic retrieval of specific semantic information.

Shared neural processes support semantic control and action understanding

Highlights • Overlap between semantic control and action understanding revealed with fMRI.• Overlap found in left inferior frontal and posterior middle temporal cortex.• Peaks for action and difficulty were spatially identical in LIFG.• Peaks for action and difficulty were distinct in occipital–temporal cortex.• Difficult trials recruited additional ventral occipital–temporal areas.

Charting the effects of TMS with fMRI : Modulation of cortical recruitment within the distributed network supporting semantic control

Semantic memory comprises our knowledge of the meanings of words and objects but only some of this knowledge is relevant at any given time. Thus, semantic control processes are needed to focus retrieval on relevant information. Research on the neural basis of semantic control has strongly implicated left inferior frontal gyrus (LIFG) but recent work suggests that a wider network supports semantic control, including left posterior middle temporal gyrus (pMTG), right inferior frontal gyrus (RIFG) and pre-supplementary motor area (pre-SMA). In the current study, we used repetitive transcranial magnetic stimulation (1 Hz offline TMS) over LIFG, immediately followed by fMRI, to examine modulation of the semantic network. We compared the effect of stimulation on judgements about strongly-associated words (dog-bone) and weaker associations (dog-beach), since previous studies have found that dominant links can be recovered largely automatically with little engagement of LIFG, while more distant connections require greater control. Even though behavioural performance was maintained in response to TMS, LIFG stimulation increased the effect of semantic control demands in pMTG and pre-SMA, relative to stimulation of a control site (occipital pole). These changes were accompanied by reduced recruitment of both the stimulated region (LIFG) and its right hemisphere homologue (RIFG), particularly for strong associations with low control requirements. Thus repetitive TMS to LIFG modulated the contribution of distributed regions to semantic judgements in two distinct ways.

An amygdala response to fearful faces with covered eyes

Findings of amygdala responsiveness to the eye region of fearful faces raise the question of whether eye widening is the only facial cue involved. We used fMRI to investigate the differential amygdala response to fearful versus neutral stimuli for faces, eyes, and for faces in which the eye region was masked. For maximum sensitivity, a block design was used, with a region of interest (ROI) centred on the amygdala which included peri-amygdalar areas. Evidence of amygdala responsiveness to fear compared to neutral stimuli was found for whole faces, eye region only, and for faces with masked eyes. The amygdala can therefore use information from facial regions other than the eyes, allowing it to respond differentially to fearful compared to neutral faces even when the eye region is hidden.

Task-based and resting-state fMRI reveal compensatory network changes following damage to left inferior frontal gyrus

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.

Semantic control deficits impair understanding of thematic relationships more than object identity

ABSTRACT Recent work has suggested a potential link between the neurocognitive mechanisms supporting the retrieval of events and thematic associations (i.e., knowledge about how concepts relate in a meaningful context) and semantic control processes that support the capacity to shape retrieval to suit the circumstances. Thematic associations and events are inherently flexible: the meaning of an item changes depending on the context (for example, lamp goes with reading, bicycle and police). Control processes might stabilise weak yet currently‐relevant interpretations during event understanding. In contrast, semantic retrieval for objects (to understand what items are, and the categories they belong to) is potentially constrained by sensory‐motor features (e.g., bright light) that change less across contexts. Semantic control and event understanding produce overlapping patterns of activation in healthy participants in left prefrontal and temporoparietal regions, but the potential causal link between these aspects of semantic cognition has not been examined. We predict that event understanding relies on semantic control, due to associations being necessarily context‐dependent and variable. We tested this hypothesis in two ways: (i) by examining thematic associations and object identity in patients with semantic aphasia, who have well‐documented deficits of semantic control following left frontoparietal stroke and (ii) using the same tasks in healthy controls under dual‐task conditions that depleted the capacity for cognitive control. The patients were impaired on both identity and thematic matching tasks, and they showed particular difficulty on non‐dominant thematic associations which required greater control over semantic retrieval. Healthy participants showed the same pattern under conditions of divided attention. These findings support the view that semantic control is necessary for organising and constraining the retrieval of thematic associations. HIGHLIGHTSThis manuscript compares performance on thematic and identity tasks.We predict that thematic tasks will require additional semantic‐executive mechanisms.Semantic Aphasia patients show particular deficits in the thematic task in relation to the identity task, particularly weak associations.Healthy subjects, in an executively demanding dual‐task, showed a similar pattern to the patients.These results support the Controlled Semantic Cognition framework, and provide evidence against the dual hub account.

When comprehension elicits incomprehension: Deterioration of semantic categorisation in the absence of stimulus repetition

Repetition improves retrieval from memory; however, under some circumstances, it can also impair performance. Separate literatures have investigated this phenomenon, including studies showing subjective loss of meaning following ‘semantic satiation’, slowed naming and categorisation when semantically related items are repeated and semantic ‘access deficits’ in aphasia. Such effects have been variously explained in terms of habituation of repeatedly accessed representations, increased interference from strongly activated competitors and long-term weight changes reflecting the suppression of non-targets on earlier trials (i.e., retrieval-induced forgetting). While studies of semantic satiation involve massed repetition of individual items, competition and weight changes at the conceptual level should elicit declining comprehension for non-repeated items: this pattern has been demonstrated for picture naming but effects in categorisation are less clear. We developed a paced serial semantic task (PSST), in which participants identified category members among distracters. Performance in healthy young adults deteriorated with ongoing retrieval for non-repeated words belonging to functional categories (e.g., picnic), taxonomic categories (e.g., animal) and feature-based categories (e.g., colour red – ‘tomato’, ‘post box’). This decline was greatest at fast presentation speeds (when there was less time to overcome competition/inhibition) and for strongly associated targets (which may have accrued more inhibition to facilitate earlier target categorisation). Deteriorating performance was also seen across words and pictures, consistent with a conceptual locus. We observed a release from deteriorating categorisation following a switch to a new category, demonstrating that this was not a general effect of time on task. Patients with semantic aphasia, who have deficient semantic control, maintained their performance throughout the categories, unlike younger adults: this finding is hard to reconcile with accounts of declining performance that propose a build-up of competition, since the patients should have had greater difficulty resolving such competition. These results instead suggest that declining performance on our goal-driven categorisation task was linked to the use of a controlled retrieval strategy by healthy young adults. Patients may not have inhibited related non-target knowledge to facilitate initial categorisation like younger volunteers, and consequently they were less vulnerable to declining comprehension in this paradigm. Together, these results demonstrate circumstances which produce declines in continuous categorisation in healthy adults.