Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes

Mollo, Giovanna; Cornelissen, Piers L.; Millman, Rebecca E.; Ellis, Andrew W.; Jefferies, Elizabeth

doi:10.1371/journal.pone.0169269

Cited by 42 publications

(66 citation statements)

References 123 publications

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“…Crucially, recurrent activity will be associated with the activation of semantic object information that will also depend on the coordinated activity within the VVP. Whilst visual object properties are predicted in alpha (VanRullen et al, 2014), semantic information may be more associated with theta activity (Halgren et al, 2015) and gamma activity (Mollo et al, 2017;Supp et al, 2007).…”

Section: Introductionmentioning

confidence: 94%

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

Clarke

Devereux

Tyler

2018

Preprint

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Object recognition requires dynamic transformations of low-level visual inputs to complex semantic representations. While this process depends on the ventral visual pathway (VVP), we lack an incremental account from low-level inputs to semantic representations, and the mechanistic details of these dynamics. Here we combine computational models of vision with semantics, and test the output of the incremental model against patterns of neural oscillations recorded with MEG in humans. Representational Similarity Analysis showed visual information was represented in alpha activity throughout the VVP, and semantic information was represented in theta activity. Furthermore, informational connectivity showed visual information travels through feedforward connections, while visual information is transformed into semantic representations through feedforward and feedback activity, centered on the anterior temporal lobe. Our research highlights that the complex transformations between visual and semantic information is driven by feedforward and recurrent dynamics resulting in object-specific semantics.

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Section: Introductionmentioning

confidence: 94%

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

Clarke

Devereux

Tyler

2018

Preprint

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“…The outputs of the three spatial filters at each point in the brain were summed to generate estimates of oscillatory power. This analysis strategy and the parameters used for the current study were similar to those used in recent MEG studies of visual word recognition, object naming and semantic processing (Wheat et al, 2010;Klein et al, 2014;Urooj, 2014;Mollo et al, 2017).…”

Section: Data Collectionmentioning

confidence: 99%

“…The time-frequency representations of total power were normalized, separately for each condition and for each participant, with respect to the mean power per frequency bin in a baseline period prior to the start of trials in that condition (-700 to -500 ms). This window length was also used in earlier studies (Mollo et al, 2017;Wheat et al, 2010;Klein et al, 2014), since it provides a compromise between the minimum length sufficient to estimate power at the lowest frequency reported here (i.e., 5Hz) and the requirement to characterise the state of the brain immediately before the onset of each trial.…”

Section: Time-frequency Analysis: Point Of Interest (Poi)mentioning

confidence: 99%

“…al., 2000), functional magnetic resonance imaging (fMRI) -particularly when magnetic susceptibility artefacts within ATL are minimised (Binney et al, 2010;Murphy et al, 2017;Visser et al,2010;, magnetoencephalography (MEG) (Lau et al, 2013;Clarke et al, 2011;Marinković et al, 2003;Fujimaki et al, 2009;Mollo et al, 2017), intracranial electrode arrays (Chan et al, 2011;Chen et al, 2016) and transcranial magnetic stimulation (TMS) Pobric et al, 2009;Jackson, Lambon Ralph & Pobric, 2016). The ATL is allied to the default mode network (DMN) in terms of connectivity and function (Binder et al, 2003;Davey et al, 2015;Wirth et al, 2011), although the maximal semantic response in ATL is not identical to the site of peak DMN connectivity (Jackson et al, 2016).…”

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confidence: 99%

“…Little is known about differences in the time-course of retrieval at these two sites -and previous work has often used electroencephalography (EEG), which may lack the spatial resolution to separately resolve signals from ATL and pMTG. MEG studies of ATL show early responses (from 120ms) that appear to reflect interactions between semantic representations and inputs (Clarke et al, 2011;Mollo et al, 2017), plus later responses (250-450ms) that are influenced by patterns of coherent conceptual retrieval across both modalities (Marinkovic et al, 2003) and multiple items (Halgren et al, 2002;Lau et al, 2013;Bemis & Pylkkänen, 2011). Moreover, a recent chronometric TMS study by Jackson et al (2015) found that the critical time point of involvement for ATL was around 400ms (although this study did not manipulate the strength of association and thus cannot identify when semantic processing in ATL is critical for the efficient retrieval of more coherent concepts).…”

mentioning

confidence: 99%

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Dynamic semantic cognition: Characterising coherent and controlled conceptual retrieval through time using magnetoencephalography and chronometric transcranial magnetic stimulation

Teige

Mollo

Millman

et al. 2017

Preprint

Self Cite

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Distinct neural processes are thought to support the retrieval of semantic information that is (i) coherent with strongly-encoded aspects of knowledge, and (ii) non-dominant yet relevant for the current task or context. While the brain regions that support coherent and controlled patterns of semantic retrieval are relatively well-characterised, the temporal dynamics of these processes are not well-understood. This study used magnetoencephalography (MEG) and dual-pulse chronometric transcranial magnetic stimulation (cTMS) in two separate experiments to examine temporal dynamics within the temporal lobe during the retrieval of strong and weak associations. MEG results revealed a dissociation within left temporal cortex: anterior temporal lobe (ATL) showed greater oscillatory response for strong than weak associations, while posterior middle temporal gyrus (pMTG) showed the reverse pattern. In the cTMS experiment, stimulation of ATL at ~150ms disrupted the efficient retrieval of strong associations, indicating a necessary role for ATL in coherent conceptual activations. Stimulation of pMTG at the onset of the second word disrupted the retrieval of weak associations, suggesting this site may maintain information about semantic context from the first word, allowing engagement of semantic control.Together these studies provide converging evidence for a functional dissociation within the temporal lobe, across both tasks and time.

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Individual word representations dissociate from linguistic context along a cortical unimodal to heteromodal gradient

Eisenhauer,

Gonzalez Alam,

Cornelissen

et al. 2024

Human Brain Mapping

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Language comprehension involves multiple hierarchical processing stages across time, space, and levels of representation. When processing a word, the sensory input is transformed into increasingly abstract representations that need to be integrated with the linguistic context. Thus, language comprehension involves both input‐driven as well as context‐dependent processes. While neuroimaging research has traditionally focused on mapping individual brain regions to the distinct underlying processes, recent studies indicate that whole‐brain distributed patterns of cortical activation might be highly relevant for cognitive functions, including language. One such pattern, based on resting‐state connectivity, is the ‘principal cortical gradient’, which dissociates sensory from heteromodal brain regions. The present study investigated the extent to which this gradient provides an organizational principle underlying language function, using a multimodal neuroimaging dataset of functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) recordings from 102 participants during sentence reading. We found that the brain response to individual representations of a word (word length, orthographic distance, and word frequency), which reflect visual; orthographic; and lexical properties, gradually increases towards the sensory end of the gradient. Although these properties showed opposite effect directions in fMRI and MEG, their association with the sensory end of the gradient was consistent across both neuroimaging modalities. In contrast, MEG revealed that properties reflecting a word's relation to its linguistic context (semantic similarity and position within the sentence) involve the heteromodal end of the gradient to a stronger extent. This dissociation between individual word and contextual properties was stable across earlier and later time windows during word presentation, indicating interactive processing of word representations and linguistic context at opposing ends of the principal gradient. To conclude, our findings indicate that the principal gradient underlies the organization of a range of linguistic representations while supporting a gradual distinction between context‐independent and context‐dependent representations. Furthermore, the gradient reveals convergent patterns across neuroimaging modalities (similar location along the gradient) in the presence of divergent responses (opposite effect directions).

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Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes

Cited by 42 publications

References 123 publications

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

Dynamic semantic cognition: Characterising coherent and controlled conceptual retrieval through time using magnetoencephalography and chronometric transcranial magnetic stimulation

Individual word representations dissociate from linguistic context along a cortical unimodal to heteromodal gradient

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