Elsevier

Cortex

Volume 134, January 2021, Pages 76-91
Cortex

Research Report
Intrinsic connectivity of anterior temporal lobe relates to individual differences in semantic retrieval for landmarks

https://doi.org/10.1016/j.cortex.2020.10.007Get rights and content

Abstract

Contemporary neuroscientific accounts suggest that ventral anterior temporal lobe (ATL) acts as a bilateral heteromodal semantic hub, which is particularly critical for the specific-level knowledge needed to recognise unique entities, such as familiar landmarks and faces. There may also be graded functional differences between left and right ATL, relating to effects of modality (linguistic versus non-linguistic) and category (e.g., knowledge of people and places). Individual differences in intrinsic connectivity from left and right ATL might be associated with variation in semantic categorisation performance across these categories and modalities. We recorded resting-state fMRI in 74 individuals and, in a separate session, examined semantic categorisation. People with greater connectivity between left and right ATL were more efficient at categorising landmarks (e.g., Eiffel Tower), especially when these were presented visually. In addition, participants who showed stronger connectivity from right than left ATL to medial occipital cortex showed more efficient semantic categorisation of landmarks regardless of modality of presentation. These results can be interpreted in terms of graded differences in the patterns of connectivity across left and right ATL, which give rise to a bilateral yet partially segregated semantic ‘hub’. More specifically, right ATL connectivity supports the efficient semantic categorisation of landmarks.

Introduction

Semantic cognition allows us to understand the world around us–including the meaning of words, objects, locations and people (Lambon Ralph et al., 2017; Patterson et al., 2007). Conceptual representations that underpin semantic performance across input modalities (e.g., words and pictures) and across different tasks are thought to be supported by the bilateral ventral anterior temporal lobes (ATL; Binney et al., 2010; Rice, Hoffman, & Lambon Ralph, 2015, 2015b). Patients with semantic dementia have degraded conceptual knowledge that is associated with bilateral ATL atrophy, while other aspects of cognition remain largely intact (Lambon Ralph et al., 2017; Patterson et al., 2007). Semantic deficits following ATL damage are most pronounced for semantic tasks that probe specific-level knowledge–including knowledge of unique entities including people, such as Barack Obama, and landmarks, such as the Eiffel Tower (Rogers et al., 2015; Tranel, 2006; Tranel et al., 1997). An influential account of ATL function suggests that this region forms a semantic “hub” drawing together different features represented within ‘spokes’ (capturing visual, valence, language and auditory inputs) to form heteromodal concepts (Patterson et al., 2007). More detailed conceptual retrieval may be needed to identify unique entities and other specific concepts within this hub (Rogers et al., 2006); in line with this, unique entities activate ATL more strongly than more general-level concepts in neuroimaging studies of healthy participants (Gorno-Tempini & Price, 2001; Grabowski et al., 2001; Ross & Olson, 2012).

Neuropsychological and neuroimaging studies suggest that semantic representations draw on a bilateral hub, implemented across both left and right ATL (Ding et al., 2020; Lambon Ralph et al., 2017; Patterson et al., 2007). Severe semantic degradation follows bilateral ATL atrophy in semantic dementia; in contrast, patients with unilateral lesions following resection for temporal lobe epilepsy have measurable yet much milder semantic deficits (Rice, Caswell, et al., 2018). This might reflect functional compensation by the intact ATL (Jung & Lambon Ralph, 2016). Neuroimaging studies with healthy participants have observed bilateral responses to semantic tasks in ATL (Visser et al., 2009), irrespective of whether words or pictures are presented (Bright et al., 2004; Tranel et al., 2005; Vandenberghe et al., 1996; Visser et al., 2012; Visser & Lambon Ralph, 2011). Inhibitory transcranial magnetic stimulation (TMS) delivered to either left or right ATL disrupts both picture and word-based semantic tasks, mimicking the pattern in semantic dementia (Pobric et al, 2007, 2010). Moreover, in line with expectations for a single semantic hub distributed across two hemispheres (cf. Schapiro et al., 2013), inhibitory TMS to left ATL leads to an increase in the response within right ATL, suggesting the non-stimulated hemisphere may compensate for functional disruption within the stimulated hemisphere (Binney & Lambon Ralph, 2015; Jung & Lambon Ralph, 2016).

There is also evidence that left and right ATL are not functionally identical. The integration of different aspects of knowledge in ATL is thought to occur in a graded connectivity-dependent fashion (Bajada et al., 2019; Binney et al., 2012), with the most heteromodal responses in ventrolateral ATL (Lambon Ralph et al., 2017; Murphy et al., 2017; Visser et al., 2012). A degree of functional specialisation across the hemispheres might reflect differential white matter connections from visual, auditory-motor, social and emotional networks to left and right ATL (Papinutto et al., 2016; Rice, Hoffman, & Lambon Ralph, 2015). Some studies have suggested a modality difference across the hemispheres–with left ATL showing stronger engagement for verbal tasks, and right ATL showing a preference for non-verbal tasks. Patients with semantic dementia who have relatively more left-sided or right-sided atrophy provide support for this suggestion (Gainotti, 2012): atrophy in right ATL correlates with difficulties on picture semantic tasks, while damage to left ATL is more strongly correlated with verbal semantic task performance (Butler et al., 2009; Mion et al., 2010). A variant of this modality view suggests that output modality is also important–damage to left ATL is particularly associated with problems in naming concepts (Lambon Ralph et al., 2001), and therefore with deficient lexical access from semantic knowledge, while right ATL is linked to poor object recognition (Damasio et al., 2004). These effects of modality across left and right ATL are most commonly reported in studies comparing semantic retrieval to people's names and faces (Gainotti, 2007, 2013; Gainotti & Marra, 2011; Luzzi et al., 2017; Snowden et al, 2012, 2017): for example, Snowden et al. (2004) found that patients with more left-lateralised atrophy had greater impairment for people's names, while patients with more right-sided atrophy had greater difficulty on semantic tasks employing faces. Given that multiple neuropsychological studies have found hemispheric differences in ATL when contrasting famous people's names and faces, individual differences in connectivity from left and right ATL in healthy participants might also relate to these aspects of semantic cognition (see below; less is currently known about modality effects for the landmark category).

An alternative account suggests that hemispheric specialisation in left and right ATL reflects semantic category, not (only) input modality–by this view, right ATL has been argued to play a larger role than left ATL in understanding social concepts and retrieving conceptual information about specific people (Zahn et al., 2007). Patients with damage to right ATL often have particular difficulties recognising faces, but there is an ongoing debate about whether these difficulties reflect impairment for faces per se (i.e., difficulty when the task involves both social stimuli and picture inputs) or a wider problem with social concepts (Gainotti, 2013; Gorno-Tempini et al., 1998; Olson et al., 2007, 2013; Ross & Olson, 2010). In addition, a few neuroimaging studies have contrasted knowledge of famous faces and names with knowledge of landmarks (since both of these categories comprise unique entities): this contrast reveals common activation for both faces and landmarks in left ATL (Gorno-Tempini & Price, 2001; Grabowski et al., 2001; Wang et al., 2016), and weaker engagement of right ATL across both categories. A recent fMRI study (Rice, Hoffman, et al., 2018) directly compared the neural response in ATL during semantic decisions about specific entities that were social (people) and non-social (landmarks). The social and non-social stimuli were presented as both words (i.e., people's names) and as pictures (i.e., faces). Both the left and right ventral ATL responded regardless of the modality or category of semantic information, although an additional bilateral region in the ATL, extending towards the temporal pole, showed stronger activation to people versus landmarks. Similarly, a meta-analysis of 97 functional neuroimaging studies (Rice, Lambon Ralph, & Hoffman, 2015) confirmed that both left and right ATL were activated across verbal and non-verbal stimuli, and social and non-social tasks. Studies involving word retrieval were more likely to report unilateral left ATL activation, while social semantic studies were more likely to observe bilateral ATL activation.

Rice and colleagues (2015b) suggested that subtle functional differences between left and right ATL are likely to reflect differential connectivity to ‘spoke’ systems–for example, stronger connectivity between right ATL and visual regions, or between left ATL and language regions. In this extension of the “graded hub account”, the bilateral semantic store shows some degree of differentiation between left and right ATL, such that distinct patterns of connectivity can explain modality effects (for example, differences between faces and names). Semantic retrieval for different categories is also thought to draw disproportionately on particular feature types–for example, visual textures and movement are critical to the animal category, while action features and hand shape are important for tools (Fernandino et al., 2016; Ishibashi et al., 2016; Liljeström et al., 2008; Mollo et al., 2018; Moss et al., 1998, 2005; Rogers et al., 2005). Consequently, this type of account is potentially able to accommodate differences in the contributions of left and right ATL to distinct semantic categories, such as people versus landmarks, as well as effects of modality. In a recent study (Gonzalez Alam et al., 2019), left ATL was more connected with other sites implicated in semantic cognition (e.g., left inferior frontal gyrus, posterior middle and inferior temporal cortex), while right ATL was more connected to visual cortex and default mode network regions, including angular gyrus and dorsomedial prefrontal cortex. Despite these differences, ATL had the most symmetrical connections within the semantic network (i.e., the highest correlations between connectivity patterns generated from left and right-hemisphere seeds), consistent with the bilateral hub theory.

Individual differences in patterns of connectivity from left and right ATL might differentially relate to the efficiency of semantic decisions about people and landmarks, presented as words and pictures. Gonzalez Alam et al. (2019) failed to observe any behavioural correlates of hemispheric differences in ATL connectivity; however, this previous study did not use tasks designed to maximise the involvement of this brain area (i.e., specific-level concepts). Studies show that individual differences between participants in the strength of intrinsic connectivity, defined according to time–series correlations in resting-state fMRI, are associated with variation in cognitive performance (Cole et al., 2014; Smith et al., 2009; Van Dijk et al., 2010), including semantic cognition (Evans et al., 2020; Gonzalez Alam et al., 2018; Mollo et al., 2016; Poerio et al., 2017; Vatansever et al., 2017; Zhang et al., 2019). Hemispheric differences in intrinsic connectivity across individuals have already been linked to semantic and spatial tasks (Gonzalez Alam et al., 2019; Sormaz et al., 2017; although these prior studies did not find associations with ATL connectivity). Individual differences in the connectivity of ATL have also been associated with semantic processing, although these studies did not examine hemispheric differences (Mollo et al., 2016; Vatansever et al., 2017). To address this gap in the literature, the current study acquired resting-state fMRI from 74 participants, who completed semantic decisions about specific people and landmarks, presented as written words and pictures (using the stimuli from Rice, Hoffman, et al., 2018) in a separate testing session following the scan. We then assessed relationships between connectivity and behavioural performance–with particular focus on whether right versus left ATL connectivity would predict performance on these different categories presented as pictures versus words.

Section snippets

Methods

This study includes analysis of intrinsic connectivity in a sample of participants who performed a resting-state scan and behavioural testing in two separate sessions. We determined our sample size based on participant availability (i.e., tested as many of the participants with resting-state data as were willing), and report all data exclusions, all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations, and all measures in

Behavioural results

Fig. 2 shows the average median reaction time, accuracy and efficiency scores in each condition of the semantic task adapted from Rice, Hoffman, et al. (2018). A two-way repeated measures ANOVA on reaction time data with category and modality as factors revealed no main effect of modality, a significant main effect of category and a category by modality interaction [Category: F (2,144) = 56.07, p < .001; Interaction: F (2,144) = 69.1, p < .001]. Post-hoc tests with Bonferroni correction showed

Discussion

This study examined the relationship between individual differences in the intrinsic connectivity of left and right ATL and performance on semantic tasks that involved (i) different modalities of presentation (pictures vs words) and (ii) knowledge of specific people versus landmarks. Previous work has suggested that while the functions of left and right ATL are more similar than they are different, there is some subtle hemispheric specialisation according to modality–in particular, patients

Author contributions

Tirso RJ Gonzalez Alam: Conceptualization, Methodology, Software, Formal analysis, Investigation, Data curation, Visualization, Writing- Original draft preparation, Writing- Reviewing and Editing.

Katya Krieger-Redwood: Methodology, Formal analysis, Investigation.

Megan Evans: Formal analysis, Investigation.

Grace E Rice: Software, Writing- Reviewing and Editing.

Jonathan Smallwood: Conceptualization, Methodology, Formal analysis, Resources, Visualization, Writing- Original draft preparation,

Funding

EJ was supported by European Research Council [FLEXSEM-771863], JS was supported by European Research Council [WANDERINGMINDS-646927], TGA was supported by the National Council of Science and Technology, Mexico [Scholarship 411361].

Open Practices

The study in this article earned an Open Materials badge for transparent practices. Materials and data for the study are available at https://neurovault.org/collections/5687/.

Declaration of competing interest

None.

Acknowledgements

We would like to thank the students that helped with data collection: Melinda Bjolseth, Sophie Colgan, Lucy Milne, Clara Scatola, Nikita Schaap, George Shone, Molly Sibson-Flood, Dragos Teodorov and Molly Wilson.

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