Broca's Area Is Not a Natural Kind

Abstract

Theories of human cognition prominently feature 'Broca's area', which causally contributes to a myriad of mental functions. However, Broca's area is not a monolithic, multipurpose unit - it is structurally and functionally heterogeneous. Some functions engaging (subsets of) this area share neurocognitive resources, whereas others rely on separable circuits. A decade of converging evidence has now illuminated a fundamental distinction between two subregions of Broca's area that likely play computationally distinct roles in cognition: one belongs to the domain-specific 'language network', the other to the domain-general 'multiple-demand (MD) network'. Claims about Broca's area should be (re)cast in terms of these (and other, as yet undetermined) functional components, to establish a cumulative research enterprise where empirical findings can be replicated and theoretical proposals can be meaningfully compared and falsified.

Keywords: Broca’s area; LIFG; articulation; domain-specificity; executive functions; language.

Figure 1.. Responses to language vs. executive demands in LIFG.

(a) Probabilistic overlap maps across a sample of 405 participants showing, for each voxel, the percentage of participants who show significant (p<0.001, uncorrected) effects for a contrast between passive reading of sentences and nonword lists (left), and a contrast between hard and easy versions of a spatial working memory task (right). (The data are projected onto a lateral view of an inflated left hemisphere of an average brain template.) These two contrasts robustly and reliably identify the language network and the multiple-demand (MD) network, respectively. The boundaries of the opercular and triangular dub-divisions of the IFG are outlined in white [148]. The boundaries within which BA44 and BA45 could fall are outlined in black [149]. The IFG contains regions responsive to the sentences>nonwords contrast, as well as distinct regions responsive to the hard>easy working memory contrast. (b) Functionally distinct regions within the IFG in individual participants. Significant effects (p<0.001, uncorrected) for the sentences>nonwords contrast (red) and hard>easy working memory contrast (blue) in the IFG of four sample brains. Activations are only shown if they fall within the probabilistic borders of BA44/BA45 (light patch) and/or the boundaries of the opercular and triangular sub-divisions of the IFG (white outlines). (c) Variability in the locations of language and MD regions in the IFG. Each column shows a different coordinate in the MNI space (circled); the top two panels show activation maps in subjects with language-selective activity in that coordinate, and the bottom two panels show activation maps in subjects with domain-general MD activity in that coordinate. The white dashed contour shows the boundaries of the opercular and triangular sub-divisions of the IFG based on [150].

Figure 2.. Two regions within Broca’s area and their associated networks.

Response profiles of functionally-defined regions within Broca’s area (top two bar graphs), separately for its language-selective and domain-general MD regions (sources of the data: [,,,,–63]). The former region responds selectively to language across modalities (reading and listening) but shows low responses to linguistically/acoustically degraded controls as well as a wide array of non- linguistic stimuli and tasks (music, arithmetic, spatial and verbal working memory, cognitive control tasks, physical and mental events, and action observation). The latter region, in contrast, scales its response with processing demands in both the linguistic domain (where degraded control materials are harder to process than intact input) and multiple, non-linguistic domains. The bottom two bar graphs show the response profiles across the rest of the language network (averaged across 4 regions) and the rest of the MD network (averaged across 18 regions). Note the similarity between the response profile of the language-selective IFG region and the language network, on the one hand, and the domain-general IFG region and the MD network, on the other hand. All regions within and outside the IFG were functionally defined in individual participants using the corresponding contrasts (Figure 1a). The locations of these functional regions were constrained to fall within large areas of cortex that contain the activations of most participants in prior studies (these areas are colored on the inflated brain images on the top-right corner of each panel).

Figure 3.. Functional co-variation between the regions within Broca’s area and their networks.

(a) Co-variation between the two regions within Broca’s area and each of the remaining functional regions in the language and MD networks, based on regional fluctuations in the BOLD signal while listening to naturalistic stories [–51]. Signal fluctuations (over time) in the language-selective IFG region correlate with fluctuations elsewhere in the language (but not MD) network; and, to a lesser extent, fluctuations in the domain-general IFG region correlate with those in other left-hemispheric MD regions. (b) Co-variation between the two regions within Broca’s area and each of the remaining functional regions in the language and MD networks based on regional effect sizes across individuals [49]. Individuals with stronger (weaker) responses in the language-selective region are likely to also exhibit strong (weak) responses in other language (but not MD) regions, and vice-versa for the domain-general region.