The meaning of language is represented in regions of the cerebral cortex collectively known as the “semantic system”. However, little of the semantic system has been mapped comprehensively, and the semantic selectivity of most regions is unknown. Here we systematically map semantic selectivity across the cortex using voxel-wise modeling of fMRI data collected while subjects listened to hours of narrative stories. We show that the semantic system is organized into intricate patterns that appear consistent across individuals. We then use a novel generative model to create a detailed semantic atlas. Our results suggest that most areas within the semantic system represent information about specific semantic domains, or groups of related concepts, and our atlas shows which domains are represented in each area. This study demonstrates that data-driven methods—commonplace in studies of human neuroanatomy and functional connectivity—provide a powerful and efficient means for mapping functional representations in the brain.
Summary Humans can see and name thousands of distinct object and action categories, so it is unlikely that each category is represented in a distinct brain area. A more efficient scheme would be to represent categories as locations in a continuous semantic space mapped smoothly across the cortical surface. To search for such a space, we used functional magnetic resonance imaging (fMRI) to measure human brain activity evoked by natural movies. We then used voxel-wise models to examine the cortical representation of 1705 object and action categories. The first few dimensions of the underlying semantic space were recovered from the fit models by principal components analysis. Projection of the recovered semantic space onto cortical flat maps shows that semantic selectivity is organized into smooth gradients that cover much of visual and non-visual cortex. Furthermore, both the recovered semantic space and the cortical organization of the space are shared across different individuals.
Speech comprehension requires that the brain extract semantic meaning from the spectral features represented at the cochlea. To investigate this process, we performed an fMRI experiment in which five men and two women passively listened to several hours of natural narrative speech. We then used voxelwise modeling to predict BOLD responses based on three different feature spaces that represent the spectral, articulatory, and semantic properties of speech. The amount of variance explained by each feature space was then assessed using a separate validation dataset. Because some responses might be explained equally well by more than one feature space, we used a variance partitioning analysis to determine the fraction of the variance that was uniquely explained by each feature space. Consistent with previous studies, we found that speech comprehension involves hierarchical representations starting in primary auditory areas and moving laterally on the temporal lobe: spectral features are found in the core of A1, mixtures of spectral and articulatory in STG, mixtures of articulatory and semantic in STS, and semantic in STS and beyond. Our data also show that both hemispheres are equally and actively involved in speech perception and interpretation. Further, responses as early in the auditory hierarchy as in STS are more correlated with semantic than spectral representations. These results illustrate the importance of using natural speech in neurolinguistic research. Our methodology also provides an efficient way to simultaneously test multiple specific hypotheses about the representations of speech without using block designs and segmented or synthetic speech.
Little is known about how attention changes the cortical representation of sensory information in humans. Based on neurophysiological evidence, we hypothesized that attention causes tuning changes to expand the representation of attended stimuli at the cost of unattended stimuli. To investigate this issue we used functional MRI (fMRI) to measure how semantic representation changes when searching for different object categories in natural movies. We find that many voxels across occipito-temporal and fronto-parietal cortex shift their tuning toward the attended category. These tuning shifts expand the representation of the attended category and of semantically-related but unattended categories, and compress the representation of categories semantically-dissimilar to the target. Attentional warping of semantic representation occurs even when the attended category is not present in the movie, thus the effect is not a target-detection artifact. These results suggest that attention dynamically alters visual representation to optimize processing of behaviorally relevant objects during natural vision.
Language encoding models help explain language processing in the human brain by learning functions that predict brain responses from the language stimuli that elicited them. Current word embedding-based approaches treat each stimulus word independently and thus ignore the influence of context on language understanding. In this work, we instead build encoding models using rich contextual representations derived from an LSTM language model. Our models show a significant improvement in encoding performance relative to state-of-the-art embeddings in nearly every brain area. By varying the amount of context used in the models and providing the models with distorted context, we show that this improvement is due to a combination of better word embeddings learned by the LSTM language model and contextual information. We are also able to use our models to map context sensitivity across the cortex. These results suggest that LSTM language models learn high-level representations that are related to representations in the human brain.
Humans have a unique ability to produce and consume rich, complex, and varied language in order to communicate ideas to one another. Still, outside of natural reading, the most common methods for studying how our brains process speech or understand language use only isolated words or simple sentences. Recent studies have upset this status quo by employing complex natural stimuli and measuring how the brain responds to language as it is used. In this article we argue that natural stimuli offer many advantages over simplified, controlled stimuli for studying how language is processed by the brain. Furthermore, the downsides of using natural language stimuli can be mitigated using modern statistical and computational techniques.
An integral part of human language is the capacity to extract meaning from spoken and written words, but the precise relationship between brain representations of information perceived by listening versus reading is unclear. Prior neuroimaging studies have shown that semantic information in spoken language is represented in multiple regions in the human cerebral cortex, while amodal semantic information appears to be represented in a few broad brain regions. However, previous studies were too insensitive to determine whether semantic representations were shared at a fine level of detail rather than merely at a coarse scale. We used fMRI to record brain activity in two separate experiments while participants listened to or read several hours of the same narrative stories, and then created voxelwise encoding models to characterize semantic selectivity in each voxel and in each individual participant. We find that semantic tuning during listening and reading are highly correlated in most semantically selective regions of cortex, and models estimated using one modality accurately predict voxel responses in the other modality. These results suggest that the representation of language semantics is independent of the sensory modality through which the semantic information is received.
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