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

Abstract

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 readily coherent and more 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 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. Left inferior frontal gyrus (IFG), a site associated with semantic control and retrieval, showed both patterns at different time points. In the cTMS experiment, stimulation of ATL at ∼150 msec 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 efficient engagement of semantic control. Together these studies provide converging evidence for a functional dissociation within the temporal lobe, across both tasks and time.

Keywords: Anterior temporal; Beamforming; Comprehension; Posterior middle temporal gyrus; Semantic memory.

Fig. 1

a) Example trials and timelines for the MEG and TMS experiments. b) Reaction time and c) accuracy data from the behavioural (gray bars) and MEG (white bars) experiments. Standard errors are corrected for repeated measures.

Fig. 2

Whole-brain beamforming results for the 25–35 Hz frequency band, showing differences in total oscillatory power between an active period following target onset and a passive period prior to each trial. The first 600 msec following presentation of target word are displayed, in 200 msec windows. Task effects were decreases in total power in all cases. The images show a t-value map, thresholded at p < .05.

Fig. 3

Total oscillatory power across the whole epoch for related trials, including both words presented in the relatedness judgement task. Presentation of the prime word (first word of the pair) is shown within white vertical lines, while presentation of the target word (second word of the pair) is illustrated within black vertical lines. Orange–brown indicates regions of power increase relative to the baseline, while green–purple indicates power decreases relative to the baseline, and yellow indicates no change from baseline.

Fig. 4

a) Percentage signal change in the strong condition, relative to baseline. b) Percentage signal change in the weak condition, relative to baseline. c) Percentage signal change between strong and weak conditions, separately for ATL, pMTG and IFG. White lines are derived from the statistical comparison between strong and weak conditions. The boundaries enclose regions fulfilling two criteria: i) percentage signal change between the strong and weak conditions is significantly different from zero (p < .05) and ii) percentage signal change computed separately for each condition is significantly different from zero for at least one of the two conditions. Yellow–red colours indicate regions of power increase relative to the baseline, while cyan–blue indicates power decreases relative to the baseline, and green indicates no change from baseline.

Fig. 5

Effect of TMS on RT for strong and weak associations. TOP ROW: RT (in msec) for the strong and weak conditions for ATL (left) and pMTG (right). RT data for the strong and weak condition for the sham site is showed in dashed lines. These plots show the raw (un-modelled) means. BOTTOM ROW: A comparison of LS means differences between strong and weak conditions in the effect of TMS. Data points above the red line indicate greater disruption for the strong condition, while data points below the red line indicate greater disruption for the weak condition. Statistically significant differences (at p < .05) between the effects of TMS on strong and weak trials are indicated with asterisks. Error bars show 95% confidence intervals.