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

TY - JOUR

T1 - Exploring the role of the posterior middle temporal gyrus in semantic cognition

T2 - Integration of anterior temporal lobe with executive processes

AU - Davey, James Michael

AU - Thompson, Hannah Elizabeth

AU - Hallam, Glyn Paul

AU - Karapanagiotidis, Theodoros

AU - Murphy, Charlotte Elizabeth

AU - De Caso, Irene

AU - Krieger-Redwood, Katya Melanie

AU - Bernhardt, Boris C

AU - Smallwood, Jonathan

AU - Jefferies, Elizabeth Alice

N1 - Copyright © 2016 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2016/8/15

Y1 - 2016/8/15

N2 - 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 analysis 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.

AB - 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 analysis 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.

KW - Default mode network

KW - Memory retrieval

KW - Multidemand network

KW - Posterior middle temporal gyrus

KW - Semantic control

KW - Verbal Learning/physiology

KW - Brain Mapping/methods

KW - Humans

KW - Mental Recall/physiology

KW - Male

KW - Concept Formation/physiology

KW - Temporal Lobe/physiology

KW - Young Adult

KW - Semantics

KW - Adolescent

KW - Adult

KW - Female

KW - Executive Function/physiology

KW - Cognition/physiology

KW - Task Performance and Analysis

KW - Nerve Net/physiology

UR - http://www.scopus.com/inward/record.url?scp=84973890041&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2016.05.051

DO - 10.1016/j.neuroimage.2016.05.051

M3 - Article

C2 - 27236083

SN - 1053-8119

VL - 137

SP - 165

EP - 177

JO - Neuroimage

JF - Neuroimage

ER -