Heterogeneity of the left temporal lobe in semantic representation and control: priming multiple versus single meanings of ambiguous words

Abstract

Semantic judgments involve both representations of meaning plus executive mechanisms that guide knowledge retrieval in a task-appropriate way. These 2 components of semantic cognition-representation and control-are commonly linked to left temporal and prefrontal cortex, respectively. This simple proposal, however, remains contentious because in most functional neuroimaging studies to date, the number of concepts being activated and the involvement of executive processes during retrieval are confounded. Using functional magnetic resonance imaging, we examined a task in which semantic representation and control demands were dissociable. Words with multiple meanings like "bank" served as targets in a double-prime paradigm, in which multiple meaning activation and maximal executive demands loaded onto different priming conditions. Anterior inferior temporal gyrus (ITG) was sensitive to the number of meanings that were retrieved, suggesting a role for this region in semantic representation, while posterior middle temporal gyrus (pMTG) and inferior frontal cortex showed greater activation in conditions that maximized executive demands. These results support a functional dissociation between left ITG and pMTG, consistent with a revised neural organization in which left prefrontal and posterior temporal areas work together to underpin aspects of semantic control.

Figure 1.

Main effects. Brain activation during (A) double priming of unambiguous targets (RR) and priming of ambiguous words in which either (B) both meanings of the homonym are primed (RRa) or (C) the dominant (Rd) or (D) the subordinate interpretation (Rs) is addressed individually. Parameter estimates (with 90% confidence interval) are extracted from coordinates at peak activation for various brain regions using SPM (for MNI coordinates, see Table 4). * = the same brain region (i.e., matched in MNI coordinates) was activated in more than one contrast: right BA 4 was activated in all conditions; right BA 19 was activated in RR, RRa, and Rs; and left BA 37 was activated in RRa and Rs. Activation is corrected for multiple comparisons (P < 0.05, cluster extent = 12 voxels).

Figure 2.

Results of the conjunction analyses. Brain activation refers to contrasts of (A) multiple versus single meaning activation of homonyms (RRa ∩ RRa > Rd ∩ RRa > Rs; exclusively masked by RR) and (B) highest versus lowest forms of semantic control (Rs ∩ Rs > Rd). Contrast estimates and 90% confidence interval are plotted for peak activation in left ITG (BA 20), LIFG (BA 44, 47), left pMTG (BA 21), and left angular gyrus (AG; BA 39) using SPM (for MNI coordinates, see Table 5). Activation is corrected for multiple comparisons (P < 0.05, cluster extent = 12 voxels).

Figure 3.

(A) Left temporal lobe activation during ambiguity resolution (i.e., ambiguous > unambiguous material, retrieval of subordinate > dominant concepts of homonyms). (B) Left temporal and inferior frontal activation during tasks of high versus low semantic control demands for ambiguous (red) and unambiguous (green) stimuli. Brain activation is superimposed onto a semi-transparent MNI template using DataViewer3D. Black dots refer to the result of the conjunction analyses, reflecting multiple versus single meaning retrieval in mid-ITG and highest versus lowest semantic control demand in pMTG and LIFG (see Table 5). Color codes in Figure 3A: red = Snijders et al. (2009), green = Zempleni et al. (2007), blue = Gennari et al. (2007), pink = Bedny et al. (2008), and yellow = Hoenig et al. (2009).