Semantic encoding during language comprehension at single-cell resolution.

From sequences of speech sounds1,2 or letters3, humans can extract rich and nuanced meaning through language. This capacity is essential for human communication. Yet, despite a growing understanding of the brain areas that support linguistic and semantic processing4-12, the derivation of linguistic meaning in neural tissue at the cellular level and over the timescale of action potentials remains largely unknown. Here we recorded from single cells in the left language-dominant prefrontal cortex as participants listened to semantically diverse sentences and naturalistic stories. By tracking their activities during natural speech processing, we discover a fine-scale cortical representation of semantic information by individual neurons. These neurons responded selectively to specific word meanings and reliably distinguished words from nonwords. Moreover, rather than responding to the words as fixed memory representations, their activities were highly dynamic, reflecting the words' meanings based on their specific sentence contexts and independent of their phonetic form. Collectively, we show how these cell ensembles accurately predicted the broad semantic categories of the words as they were heard in real time during speech and how they tracked the sentences in which they appeared. We also show how they encoded the hierarchical structure of these meaning representations and how these representations mapped onto the cell population. Together, these findings reveal a finely detailed cortical organization of semantic representations at the neuron scale in humans and begin to illuminate the cellular-level processing of meaning during language comprehension.

Linguistic inputs must be syntactically parsable to fully engage the language network.

Human language comprehension is remarkably robust to ill-formed inputs (e.g., word transpositions). This robustness has led some to argue that syntactic parsing is largely an illusion, and that incremental comprehension is more heuristic, shallow, and semantics-based than is often assumed. However, the available data are also consistent with the possibility that humans always perform rule-like symbolic parsing and simply deploy error correction mechanisms to reconstruct ill-formed inputs when needed. We put these hypotheses to a new stringent test by examining brain responses to a) stimuli that should pose a challenge for syntactic reconstruction but allow for complex meanings to be built within local contexts through associative/shallow processing (sentences presented in a backward word order), and b) grammatically well-formed but semantically implausible sentences that should impede semantics-based heuristic processing. Using a novel behavioral syntactic reconstruction paradigm, we demonstrate that backward-presented sentences indeed impede the recovery of grammatical structure during incremental comprehension. Critically, these backward-presented stimuli elicit a relatively low response in the language areas, as measured with fMRI. In contrast, semantically implausible but grammatically well-formed sentences elicit a response in the language areas similar in magnitude to naturalistic (plausible) sentences. In other words, the ability to build syntactic structures during incremental language processing is both necessary and sufficient to fully engage the language network. Taken together, these results provide strongest to date support for a generalized reliance of human language comprehension on syntactic parsing.

Language is primarily a tool for communication rather than thought.

Language is a defining characteristic of our species, but the function, or functions, that it serves has been debated for centuries. Here we bring recent evidence from neuroscience and allied disciplines to argue that in modern humans, language is a tool for communication, contrary to a prominent view that we use language for thinking. We begin by introducing the brain network that supports linguistic ability in humans. We then review evidence for a double dissociation between language and thought, and discuss several properties of language that suggest that it is optimized for communication. We conclude that although the emergence of language has unquestionably transformed human culture, language does not appear to be a prerequisite for complex thought, including symbolic thought. Instead, language is a powerful tool for the transmission of cultural knowledge; it plausibly co-evolved with our thinking and reasoning capacities, and only reflects, rather than gives rise to, the signature sophistication of human cognition.

The Language Network Reliably "Tracks" Naturalistic Meaningful Nonverbal Stimuli.

The language network, comprised of brain regions in the left frontal and temporal cortex, responds robustly and reliably during language comprehension but shows little or no response during many nonlinguistic cognitive tasks (e.g., Fedorenko & Blank, 2020). However, one domain whose relationship with language remains debated is semantics-our conceptual knowledge of the world. Given that the language network responds strongly to meaningful linguistic stimuli, could some of this response be driven by the presence of rich conceptual representations encoded in linguistic inputs? In this study, we used a naturalistic cognition paradigm to test whether the cognitive and neural resources that are responsible for language processing are also recruited for processing semantically rich nonverbal stimuli. To do so, we measured BOLD responses to a set of ∼5-minute-long video and audio clips that consisted of meaningful event sequences but did not contain any linguistic content. We then used the intersubject correlation (ISC) approach (Hasson et al., 2004) to examine the extent to which the language network "tracks" these stimuli, that is, exhibits stimulus-related variation. Across all the regions of the language network, meaningful nonverbal stimuli elicited reliable ISCs. These ISCs were higher than the ISCs elicited by semantically impoverished nonverbal stimuli (e.g., a music clip), but substantially lower than the ISCs elicited by linguistic stimuli. Our results complement earlier findings from controlled experiments (e.g., Ivanova et al., 2021) in providing further evidence that the language network shows some sensitivity to semantic content in nonverbal stimuli.

Precision fMRI reveals that the language network exhibits adult-like left-hemispheric lateralization by 4 years of age.

Left hemisphere damage in adulthood often leads to linguistic deficits, but many cases of early damage leave linguistic processing preserved, and a functional language system can develop in the right hemisphere. To explain this early apparent equipotentiality of the two hemispheres for language, some have proposed that the language system is bilateral during early development and only becomes left-lateralized with age. We examined language lateralization using functional magnetic resonance imaging with two large pediatric cohorts (total n=273 children ages 4-16; n=107 adults). Strong, adult-level left-hemispheric lateralization (in activation volume and response magnitude) was evident by age 4. Thus, although the right hemisphere can take over language function in some cases of early brain damage, and although some features of the language system do show protracted development (magnitude of language response and strength of inter-regional correlations in the language network), the left-hemisphere bias for language is robustly present by 4 years of age. These results call for alternative accounts of early equipotentiality of the two hemispheres for language.

Artificial Neural Network Language Models Predict Human Brain Responses to Language Even After a Developmentally Realistic Amount of Training.

Artificial neural networks have emerged as computationally plausible models of human language processing. A major criticism of these models is that the amount of training data they receive far exceeds that of humans during language learning. Here, we use two complementary approaches to ask how the models' ability to capture human fMRI responses to sentences is affected by the amount of training data. First, we evaluate GPT-2 models trained on 1 million, 10 million, 100 million, or 1 billion words against an fMRI benchmark. We consider the 100-million-word model to be developmentally plausible in terms of the amount of training data given that this amount is similar to what children are estimated to be exposed to during the first 10 years of life. Second, we test the performance of a GPT-2 model trained on a 9-billion-token dataset to reach state-of-the-art next-word prediction performance on the human benchmark at different stages during training. Across both approaches, we find that (i) the models trained on a developmentally plausible amount of data already achieve near-maximal performance in capturing fMRI responses to sentences. Further, (ii) lower perplexity-a measure of next-word prediction performance-is associated with stronger alignment with human data, suggesting that models that have received enough training to achieve sufficiently high next-word prediction performance also acquire representations of sentences that are predictive of human fMRI responses. In tandem, these findings establish that although some training is necessary for the models' predictive ability, a developmentally realistic amount of training (∼100 million words) may suffice.

Lexical-Semantic Content, Not Syntactic Structure, Is the Main Contributor to ANN-Brain Similarity of fMRI Responses in the Language Network.

Representations from artificial neural network (ANN) language models have been shown to predict human brain activity in the language network. To understand what aspects of linguistic stimuli contribute to ANN-to-brain similarity, we used an fMRI data set of responses to n = 627 naturalistic English sentences (Pereira et al., 2018) and systematically manipulated the stimuli for which ANN representations were extracted. In particular, we (i) perturbed sentences' word order, (ii) removed different subsets of words, or (iii) replaced sentences with other sentences of varying semantic similarity. We found that the lexical-semantic content of the sentence (largely carried by content words) rather than the sentence's syntactic form (conveyed via word order or function words) is primarily responsible for the ANN-to-brain similarity. In follow-up analyses, we found that perturbation manipulations that adversely affect brain predictivity also lead to more divergent representations in the ANN's embedding space and decrease the ANN's ability to predict upcoming tokens in those stimuli. Further, results are robust as to whether the mapping model is trained on intact or perturbed stimuli and whether the ANN sentence representations are conditioned on the same linguistic context that humans saw. The critical result-that lexical-semantic content is the main contributor to the similarity between ANN representations and neural ones-aligns with the idea that the goal of the human language system is to extract meaning from linguistic strings. Finally, this work highlights the strength of systematic experimental manipulations for evaluating how close we are to accurate and generalizable models of the human language network.

Language in Brains, Minds, and Machines.

It has long been argued that only humans could produce and understand language. But now, for the first time, artificial language models (LMs) achieve this feat. Here we survey the new purchase LMs are providing on the question of how language is implemented in the brain. We discuss why, a priori, LMs might be expected to share similarities with the human language system. We then summarize evidence that LMs represent linguistic information similarly enough to humans to enable relatively accurate brain encoding and decoding during language processing. Finally, we examine which LM properties-their architecture, task performance, or training-are critical for capturing human neural responses to language and review studies using LMs as in silico model organisms for testing hypotheses about language. These ongoing investigations bring us closer to understanding the representations and processes that underlie our ability to comprehend sentences and express thoughts in language.

The language network as a natural kind within the broader landscape of the human brain.

Language behaviour is complex, but neuroscientific evidence disentangles it into distinct components supported by dedicated brain areas or networks. In this Review, we describe the 'core' language network, which includes left-hemisphere frontal and temporal areas, and show that it is strongly interconnected, independent of input and output modalities, causally important for language and language-selective. We discuss evidence that this language network plausibly stores language knowledge and supports core linguistic computations related to accessing words and constructions from memory and combining them to interpret (decode) or generate (encode) linguistic messages. We emphasize that the language network works closely with, but is distinct from, both lower-level - perceptual and motor - mechanisms and higher-level systems of knowledge and reasoning. The perceptual and motor mechanisms process linguistic signals, but, in contrast to the language network, are sensitive only to these signals' surface properties, not their meanings; the systems of knowledge and reasoning (such as the system that supports social reasoning) are sometimes engaged during language use but are not language-selective. This Review lays a foundation both for in-depth investigations of these different components of the language processing pipeline and for probing inter-component interactions.

Distributed Sensitivity to Syntax and Semantics throughout the Language Network.

Human language is expressive because it is compositional: The meaning of a sentence (semantics) can be inferred from its structure (syntax). It is commonly believed that language syntax and semantics are processed by distinct brain regions. Here, we revisit this claim using precision fMRI methods to capture separation or overlap of function in the brains of individual participants. Contrary to prior claims, we find distributed sensitivity to both syntax and semantics throughout a broad frontotemporal brain network. Our results join a growing body of evidence for an integrated network for language in the human brain within which internal specialization is primarily a matter of degree rather than kind, in contrast with influential proposals that advocate distinct specialization of different brain areas for different types of linguistic functions.

Functional characterization of the language network of polyglots and hyperpolyglots with precision fMRI.

How do polyglots-individuals who speak five or more languages-process their languages, and what can this population tell us about the language system? Using fMRI, we identified the language network in each of 34 polyglots (including 16 hyperpolyglots with knowledge of 10+ languages) and examined its response to the native language, non-native languages of varying proficiency, and unfamiliar languages. All language conditions engaged all areas of the language network relative to a control condition. Languages that participants rated as higher proficiency elicited stronger responses, except for the native language, which elicited a similar or lower response than a non-native language of similar proficiency. Furthermore, unfamiliar languages that were typologically related to the participants' high-to-moderate-proficiency languages elicited a stronger response than unfamiliar unrelated languages. The results suggest that the language network's response magnitude scales with the degree of engagement of linguistic computations (e.g. related to lexical access and syntactic-structure building). We also replicated a prior finding of weaker responses to native language in polyglots than non-polyglot bilinguals. These results contribute to our understanding of how multiple languages coexist within a single brain and provide new evidence that the language network responds more strongly to stimuli that more fully engage linguistic computations.

High-level language brain regions process sublexical regularities.

A network of left frontal and temporal brain regions supports language processing. This "core" language network stores our knowledge of words and constructions as well as constraints on how those combine to form sentences. However, our linguistic knowledge additionally includes information about phonemes and how they combine to form phonemic clusters, syllables, and words. Are phoneme combinatorics also represented in these language regions? Across five functional magnetic resonance imaging experiments, we investigated the sensitivity of high-level language processing brain regions to sublexical linguistic regularities by examining responses to diverse nonwords-sequences of phonemes that do not constitute real words (e.g. punes, silory, flope). We establish robust responses in the language network to visually (experiment 1a, n = 605) and auditorily (experiments 1b, n = 12, and 1c, n = 13) presented nonwords. In experiment 2 (n = 16), we find stronger responses to nonwords that are more well-formed, i.e. obey the phoneme-combinatorial constraints of English. Finally, in experiment 3 (n = 14), we provide suggestive evidence that the responses in experiments 1 and 2 are not due to the activation of real words that share some phonology with the nonwords. The results suggest that sublexical regularities are stored and processed within the same fronto-temporal network that supports lexical and syntactic processes.

Dissociating language and thought in large language models.

Large language models (LLMs) have come closest among all models to date to mastering human language, yet opinions about their linguistic and cognitive capabilities remain split. Here, we evaluate LLMs using a distinction between formal linguistic competence (knowledge of linguistic rules and patterns) and functional linguistic competence (understanding and using language in the world). We ground this distinction in human neuroscience, which has shown that formal and functional competence rely on different neural mechanisms. Although LLMs are surprisingly good at formal competence, their performance on functional competence tasks remains spotty and often requires specialized fine-tuning and/or coupling with external modules. We posit that models that use language in human-like ways would need to master both of these competence types, which, in turn, could require the emergence of separate mechanisms specialized for formal versus functional linguistic competence.

Driving and suppressing the human language network using large language models.

Transformer models such as GPT generate human-like language and are predictive of human brain responses to language. Here, using functional-MRI-measured brain responses to 1,000 diverse sentences, we first show that a GPT-based encoding model can predict the magnitude of the brain response associated with each sentence. We then use the model to identify new sentences that are predicted to drive or suppress responses in the human language network. We show that these model-selected novel sentences indeed strongly drive and suppress the activity of human language areas in new individuals. A systematic analysis of the model-selected sentences reveals that surprisal and well-formedness of linguistic input are key determinants of response strength in the language network. These results establish the ability of neural network models to not only mimic human language but also non-invasively control neural activity in higher-level cortical areas, such as the language network.

Functional characterization of the language network of polyglots and hyperpolyglots with precision fMRI.

How do polyglots-individuals who speak five or more languages-process their languages, and what can this population tell us about the language system? Using fMRI, we identified the language network in each of 34 polyglots (including 16 hyperpolyglots with knowledge of 10+ languages) and examined its response to the native language, non-native languages of varying proficiency, and unfamiliar languages. All language conditions engaged all areas of the language network relative to a control condition. Languages that participants rated as higher-proficiency elicited stronger responses, except for the native language, which elicited a similar or lower response than a non-native language of similar proficiency. Furthermore, unfamiliar languages that were typologically related to the participants' high-to-moderate-proficiency languages elicited a stronger response than unfamiliar unrelated languages. The results suggest that the language network's response magnitude scales with the degree of engagement of linguistic computations (e.g., related to lexical access and syntactic-structure building). We also replicated a prior finding of weaker responses to native language in polyglots than non-polyglot bilinguals. These results contribute to our understanding of how multiple languages co-exist within a single brain and provide new evidence that the language network responds more strongly to stimuli that more fully engage linguistic computations.

Let's move forward: Image-computable models and a common model evaluation scheme are prerequisites for a scientific understanding of human vision.

In the target article, Bowers et al. dispute deep artificial neural network (ANN) models as the currently leading models of human vision without producing alternatives. They eschew the use of public benchmarking platforms to compare vision models with the brain and behavior, and they advocate for a fragmented, phenomenon-specific modeling approach. These are unconstructive to scientific progress. We outline how the Brain-Score community is moving forward to add new model-to-human comparisons to its community-transparent suite of benchmarks.

Event Knowledge in Large Language Models: The Gap Between the Impossible and the Unlikely.

Word co-occurrence patterns in language corpora contain a surprising amount of conceptual knowledge. Large language models (LLMs), trained to predict words in context, leverage these patterns to achieve impressive performance on diverse semantic tasks requiring world knowledge. An important but understudied question about LLMs' semantic abilities is whether they acquire generalized knowledge of common events. Here, we test whether five pretrained LLMs (from 2018's BERT to 2023's MPT) assign a higher likelihood to plausible descriptions of agent-patient interactions than to minimally different implausible versions of the same event. Using three curated sets of minimal sentence pairs (total n = 1215), we found that pretrained LLMs possess substantial event knowledge, outperforming other distributional language models. In particular, they almost always assign a higher likelihood to possible versus impossible events (The teacher bought the laptop vs. The laptop bought the teacher). However, LLMs show less consistent preferences for likely versus unlikely events (The nanny tutored the boy vs. The boy tutored the nanny). In follow-up analyses, we show that (i) LLM scores are driven by both plausibility and surface-level sentence features, (ii) LLM scores generalize well across syntactic variants (active vs. passive constructions) but less well across semantic variants (synonymous sentences), (iii) some LLM errors mirror human judgment ambiguity, and (iv) sentence plausibility serves as an organizing dimension in internal LLM representations. Overall, our results show that important aspects of event knowledge naturally emerge from distributional linguistic patterns, but also highlight a gap between representations of possible/impossible and likely/unlikely events.

Grammatical cues to subjecthood are redundant in a majority of simple clauses across languages.

Grammatical cues are sometimes redundant with word meanings in natural language. For instance, English word order rules constrain the word order of a sentence like "The dog chewed the bone" even though the status of "dog" as subject and "bone" as object can be inferred from world knowledge and plausibility. Quantifying how often this redundancy occurs, and how the level of redundancy varies across typologically diverse languages, can shed light on the function and evolution of grammar. To that end, we performed a behavioral experiment in English and Russian and a cross-linguistic computational analysis measuring the redundancy of grammatical cues in transitive clauses extracted from corpus text. English and Russian speakers (n = 484) were presented with subjects, verbs, and objects (in random order and with morphological markings removed) extracted from naturally occurring sentences and were asked to identify which noun is the subject of the action. Accuracy was high in both languages (∼89% in English, ∼87% in Russian). Next, we trained a neural network machine classifier on a similar task: predicting which nominal in a subject-verb-object triad is the subject. Across 30 languages from eight language families, performance was consistently high: a median accuracy of 87%, comparable to the accuracy observed in the human experiments. The conclusion is that grammatical cues such as word order are necessary to convey subjecthood and objecthood in a minority of naturally occurring transitive clauses; nevertheless, they can (a) provide an important source of redundancy and (b) are crucial for conveying intended meaning that cannot be inferred from the words alone, including descriptions of human interactions, where roles are often reversible (e.g., Ray helped Lu/Lu helped Ray), and expressing non-prototypical meanings (e.g., "The bone chewed the dog.").