Direct physiologic evidence of a heteromodal convergence region for proper naming in human left anterior temporal lobe

Abstract

Retrieving the names of friends, loved ones, and famous people is a fundamental human ability. This ability depends on the left anterior temporal lobe (ATL), where lesions can be associated with impaired naming of people regardless of modality (e.g., picture or voice). This finding has led to the idea that the left ATL is a modality-independent convergence region for proper naming. Hypotheses for how proper-name dispositions are organized within the left ATL include both a single modality-independent (heteromodal) convergence region and spatially discrete modality-dependent (unimodal) regions. Here we show direct electrophysiologic evidence that the left ATL is heteromodal for proper-name retrieval. Using intracranial recordings placed directly on the surface of the left ATL in human subjects, we demonstrate nearly identical responses to picture and voice stimuli of famous U.S. politicians during a naming task. Our results demonstrate convergent and robust large-scale neurophysiologic responses to picture and voice naming in the human left ATL. This finding supports the idea of heteromodal (i.e., transmodal) dispositions for proper naming in the left ATL.

Keywords: electrocorticography; language; naming; temporal pole.

Figure 1.

Methods for performing intracranial recordings from the human ATL and experimental task paradigms. a, Schematic of a customized ATL electrode array that is implanted clinically for seizure localization and provides dense coverage of the human ATL. b, Intraoperative photograph showing placement of intracranial electrodes for seizure localization and cognitive mapping. In this particular example, the ATL electrode array is sectioned in half to preserve a vein on the basal surface of the temporal lobe. c, Schematic depiction of picture-naming and voice-naming tasks.

Figure 2.

Responses from representative sites demonstrating unimodal activation of pFG (X) during picture naming and STG (Y) during voice naming, but heteromodal activation of the left ATL (Z) for both picture and voice naming. a, CT-MR coregistered brain renderings demonstrating location of the implanted electrode arrays and the three representative sites on the brain of subject L206. b, Time–frequency plots of ERBP measured from representative sites on pFG (X), STG (Y), and ATL (Z).

Figure 3.

Sites within the three anatomical regions of interest (pFG, STG, and ATL, shown by red, green, and blue circles, respectively) in the three experimental subjects. Open circles denote electrode sites that were beyond the regions of interest; data from these sites were excluded from the analyses.

Figure 4.

Spectral profile of ERBP during picture (left) and voice naming (right) of proper nouns in pFG, STG, and ATL averaged across all subjects. Thick lines and shaded areas represent mean ERBP across ECoG frequencies and its 95% confidence interval, respectively. Second x-axis shows conventional ECoG frequency bands [theta (θ), 4–8 Hz; alpha (α), 8–14 Hz; beta (β), 14–30 Hz; gamma (γ), 30–70 Hz; high gamma (γ_high), 70–150 Hz]. ECoG frequency ranges that correspond to ERBP increases beyond the lower limit of the 95% confidence interval are shown as horizontal color bars.

Figure 5.

Spatial distribution of beta ERBP responses from the ATL. Sites that exhibited significant responses during picture naming and voice naming are shown in magenta and cyan, respectively. Open circles denote recording sites that were included in the analysis on anatomical grounds (Fig. 3), but did not feature significant beta response to either stimulus. Half of responsive electrode sites exhibited a heteromodal response pattern (i.e., significant induced power for both picture and voice naming). The time course of beta ERBP responses during picture and voice naming is plotted for three representative heteromodal sites (dashed circles) in magenta and cyan, respectively. Thick lines and shaded areas represent mean ERBP across ECoG frequencies and its 95% confidence interval, respectively.

Figure 6.

Spatial distribution of high-gamma ERBP responses from the ATL, pFG, and STG. Sites that exhibited significant responses during picture naming and voice naming are shown in magenta and cyan, respectively. Open circles represent recording sites included in analysis, but not showing significant high-gamma-band responses. There were no significant heteromodal high-gamma responses from ATL cortex. All three subjects had heteromodal high-gamma response sites on the posterolateral temporal lobe, perhaps representing the classically described Wernicke's area (Miller et al., 2011).