Cortical Face-Selective Responses Emerge Early in Human Infancy.

In human adults, multiple cortical regions respond robustly to faces, including the occipital face area (OFA) and fusiform face area (FFA), implicated in face perception, and the superior temporal sulcus (STS) and medial prefrontal cortex (MPFC), implicated in higher level social functions. When in development does face selectivity arise in each of these regions? Here, we combined two awake infant functional magnetic resonance imaging (fMRI) datasets to create a sample size twice the size of previous reports (n = 65 infants, 2.6-9.6 months). Infants watched movies of faces, bodies, objects, and scenes while fMRI data were collected. Despite variable amounts of data from each infant, individual subject whole-brain activation maps revealed responses to faces compared to non-face visual categories in the approximate location of OFA, FFA, STS, and MPFC. To determine the strength and nature of face selectivity in these regions, we used cross-validated functional region of interest (fROI) analyses. Across this larger sample size, face responses in OFA, FFA, STS, and MPFC were significantly greater than responses to bodies, objects, and scenes. Even the youngest infants (2-5 months) showed significantly face-selective responses in FFA, STS, and MPFC, but not OFA. These results demonstrate that face selectivity is present in multiple cortical regions within months of birth, providing powerful constraints on theories of cortical development.Significance Statement Social cognition often begins with face perception. In adults, several cortical regions respond robustly to faces, yet little is known about when and how these regions first arise in development. To test whether face selectivity changes in the first year of life, we combined two datasets, doubling the sample size relative to previous reports. In the approximate location of the fusiform face area (FFA), superior temporal sulcus (STS), and medial prefrontal cortex (MPFC) but not occipital face area (OFA), face selectivity was present in the youngest group. These findings demonstrate that face-selective responses are present across multiple lobes of the brain very early in life.

Representation of navigational affordances and ego-motion in the occipital place area.

Humans effortlessly use vision to plan and guide navigation through the local environment, or "scene". A network of three cortical regions responds selectively to visual scene information, including the occipital (OPA), parahippocampal (PPA), and medial place areas (MPA) - but how this network supports visually-guided navigation is unclear. Recent evidence suggests that one region in particular, the OPA, supports visual representations for navigation, while PPA and MPA support other aspects of scene processing. However, most previous studies tested only static scene images, which lack the dynamic experience of navigating through scenes. We used dynamic movie stimuli to test whether OPA, PPA, and MPA represent two critical kinds of navigationally-relevant information: navigational affordances (e.g., can I walk to the left, right, or both?) and ego-motion (e.g., am I walking forward or backward? turning left or right?). We found that OPA is sensitive to both affordances and ego-motion, as well as the conflict between these cues - e.g., turning toward versus away from an open doorway. These effects were significantly weaker or absent in PPA and MPA. Responses in OPA were also dissociable from those in early visual cortex, consistent with the idea that OPA responses are not merely explained by lower-level visual features. OPA responses to affordances and ego-motion were stronger in the contralateral than ipsilateral visual field, suggesting that OPA encodes navigationally relevant information within an egocentric reference frame. Taken together, these results support the hypothesis that OPA contains visual representations that are useful for planning and guiding navigation through scenes.

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.

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.

Behavioral signatures of face perception emerge in deep neural networks optimized for face recognition.

Human face recognition is highly accurate and exhibits a number of distinctive and well-documented behavioral "signatures" such as the use of a characteristic representational space, the disproportionate performance cost when stimuli are presented upside down, and the drop in accuracy for faces from races the participant is less familiar with. These and other phenomena have long been taken as evidence that face recognition is "special". But why does human face perception exhibit these properties in the first place? Here, we use deep convolutional neural networks (CNNs) to test the hypothesis that all of these signatures of human face perception result from optimization for the task of face recognition. Indeed, as predicted by this hypothesis, these phenomena are all found in CNNs trained on face recognition, but not in CNNs trained on object recognition, even when additionally trained to detect faces while matching the amount of face experience. To test whether these signatures are in principle specific to faces, we optimized a CNN on car discrimination and tested it on upright and inverted car images. As we found for face perception, the car-trained network showed a drop in performance for inverted vs. upright cars. Similarly, CNNs trained on inverted faces produced an inverted face inversion effect. These findings show that the behavioral signatures of human face perception reflect and are well explained as the result of optimization for the task of face recognition, and that the nature of the computations underlying this task may not be so special after all.

Preliminary evidence for selective cortical responses to music in one-month-old infants.

Prior studies have observed selective neural responses in the adult human auditory cortex to music and speech that cannot be explained by the differing lower-level acoustic properties of these stimuli. Does infant cortex exhibit similarly selective responses to music and speech shortly after birth? To answer this question, we attempted to collect functional magnetic resonance imaging (fMRI) data from 45 sleeping infants (2.0- to 11.9-weeks-old) while they listened to monophonic instrumental lullabies and infant-directed speech produced by a mother. To match acoustic variation between music and speech sounds we (1) recorded music from instruments that had a similar spectral range as female infant-directed speech, (2) used a novel excitation-matching algorithm to match the cochleagrams of music and speech stimuli, and (3) synthesized "model-matched" stimuli that were matched in spectrotemporal modulation statistics to (yet perceptually distinct from) music or speech. Of the 36 infants we collected usable data from, 19 had significant activations to sounds overall compared to scanner noise. From these infants, we observed a set of voxels in non-primary auditory cortex (NPAC) but not in Heschl's Gyrus that responded significantly more to music than to each of the other three stimulus types (but not significantly more strongly than to the background scanner noise). In contrast, our planned analyses did not reveal voxels in NPAC that responded more to speech than to model-matched speech, although other unplanned analyses did. These preliminary findings suggest that music selectivity arises within the first month of life. A video abstract of this article can be viewed at https://youtu.be/c8IGFvzxudk. RESEARCH HIGHLIGHTS: Responses to music, speech, and control sounds matched for the spectrotemporal modulation-statistics of each sound were measured from 2- to 11-week-old sleeping infants using fMRI. Auditory cortex was significantly activated by these stimuli in 19 out of 36 sleeping infants. Selective responses to music compared to the three other stimulus classes were found in non-primary auditory cortex but not in nearby Heschl's Gyrus. Selective responses to speech were not observed in planned analyses but were observed in unplanned, exploratory analyses.

CNNs reveal the computational implausibility of the expertise hypothesis.

Face perception has long served as a classic example of domain specificity of mind and brain. But an alternative "expertise" hypothesis holds that putatively face-specific mechanisms are actually domain-general, and can be recruited for the perception of other objects of expertise (e.g., cars for car experts). Here, we demonstrate the computational implausibility of this hypothesis: Neural network models optimized for generic object categorization provide a better foundation for expert fine-grained discrimination than do models optimized for face recognition.

Using artificial neural networks to ask 'why' questions of minds and brains.

Neuroscientists have long characterized the properties and functions of the nervous system, and are increasingly succeeding in answering how brains perform the tasks they do. But the question 'why' brains work the way they do is asked less often. The new ability to optimize artificial neural networks (ANNs) for performance on human-like tasks now enables us to approach these 'why' questions by asking when the properties of networks optimized for a given task mirror the behavioral and neural characteristics of humans performing the same task. Here we highlight the recent success of this strategy in explaining why the visual and auditory systems work the way they do, at both behavioral and neural levels.

A highly selective response to food in human visual cortex revealed by hypothesis-free voxel decomposition.

Prior work has identified cortical regions selectively responsive to specific categories of visual stimuli. However, this hypothesis-driven work cannot reveal how prominent these category selectivities are in the overall functional organization of the visual cortex, or what others might exist that scientists have not thought to look for. Furthermore, standard voxel-wise tests cannot detect distinct neural selectivities that coexist within voxels. To overcome these limitations, we used data-driven voxel decomposition methods to identify the main components underlying fMRI responses to thousands of complex photographic images. Our hypothesis-neutral analysis rediscovered components selective for faces, places, bodies, and words, validating our method and showing that these selectivities are dominant features of the ventral visual pathway. The analysis also revealed an unexpected component with a distinct anatomical distribution that responded highly selectively to images of food. Alternative accounts based on low- to mid-level visual features, such as color, shape, or texture, failed to account for the food selectivity of this component. High-throughput testing and control experiments with matched stimuli on a highly accurate computational model of this component confirm its selectivity for food. We registered our methods and hypotheses before replicating them on held-out participants and in a novel dataset. These findings demonstrate the power of data-driven methods and show that the dominant neural responses of the ventral visual pathway include not only selectivities for faces, scenes, bodies, and words but also the visually heterogeneous category of food, thus constraining accounts of when and why functional specialization arises in the cortex.

Invariant representation of physical stability in the human brain.

Successful engagement with the world requires the ability to predict what will happen next. Here, we investigate how the brain makes a fundamental prediction about the physical world: whether the situation in front of us is stable, and hence likely to stay the same, or unstable, and hence likely to change in the immediate future. Specifically, we ask if judgments of stability can be supported by the kinds of representations that have proven to be highly effective at visual object recognition in both machines and brains, or instead if the ability to determine the physical stability of natural scenes may require generative algorithms that simulate the physics of the world. To find out, we measured responses in both convolutional neural networks (CNNs) and the brain (using fMRI) to natural images of physically stable versus unstable scenarios. We find no evidence for generalizable representations of physical stability in either standard CNNs trained on visual object and scene classification (ImageNet), or in the human ventral visual pathway, which has long been implicated in the same process. However, in frontoparietal regions previously implicated in intuitive physical reasoning we find both scenario-invariant representations of physical stability, and higher univariate responses to unstable than stable scenes. These results demonstrate abstract representations of physical stability in the dorsal but not ventral pathway, consistent with the hypothesis that the computations underlying stability entail not just pattern classification but forward physical simulation.

Using child-friendly movie stimuli to study the development of face, place, and object regions from age 3 to 12 years.

Scanning young children while they watch short, engaging, commercially-produced movies has emerged as a promising approach for increasing data retention and quality. Movie stimuli also evoke a richer variety of cognitive processes than traditional experiments, allowing the study of multiple aspects of brain development simultaneously. However, because these stimuli are uncontrolled, it is unclear how effectively distinct profiles of brain activity can be distinguished from the resulting data. Here we develop an approach for identifying multiple distinct subject-specific Regions of Interest (ssROIs) using fMRI data collected during movie-viewing. We focused on the test case of higher-level visual regions selective for faces, scenes, and objects. Adults (N = 13) were scanned while viewing a 5.6-min child-friendly movie, as well as a traditional localizer experiment with blocks of faces, scenes, and objects. We found that just 2.7 min of movie data could identify subject-specific face, scene, and object regions. While successful, movie-defined ssROIS still showed weaker domain selectivity than traditional ssROIs. Having validated our approach in adults, we then used the same methods on movie data collected from 3 to 12-year-old children (N = 122). Movie response timecourses in 3-year-old children's face, scene, and object regions were already significantly and specifically predicted by timecourses from the corresponding regions in adults. We also found evidence of continued developmental change, particularly in the face-selective posterior superior temporal sulcus. Taken together, our results reveal both early maturity and functional change in face, scene, and object regions, and more broadly highlight the promise of short, child-friendly movies for developmental cognitive neuroscience.

Brain-like functional specialization emerges spontaneously in deep neural networks.

The human brain contains multiple regions with distinct, often highly specialized functions, from recognizing faces to understanding language to thinking about what others are thinking. However, it remains unclear why the cortex exhibits this high degree of functional specialization in the first place. Here, we consider the case of face perception using artificial neural networks to test the hypothesis that functional segregation of face recognition in the brain reflects a computational optimization for the broader problem of visual recognition of faces and other visual categories. We find that networks trained on object recognition perform poorly on face recognition and vice versa and that networks optimized for both tasks spontaneously segregate themselves into separate systems for faces and objects. We then show functional segregation to varying degrees for other visual categories, revealing a widespread tendency for optimization (without built-in task-specific inductive biases) to lead to functional specialization in machines and, we conjecture, also brains.

A neural population selective for song in human auditory cortex.

How is music represented in the brain? While neuroimaging has revealed some spatial segregation between responses to music versus other sounds, little is known about the neural code for music itself. To address this question, we developed a method to infer canonical response components of human auditory cortex using intracranial responses to natural sounds, and further used the superior coverage of fMRI to map their spatial distribution. The inferred components replicated many prior findings, including distinct neural selectivity for speech and music, but also revealed a novel component that responded nearly exclusively to music with singing. Song selectivity was not explainable by standard acoustic features, was located near speech- and music-selective responses, and was also evident in individual electrodes. These results suggest that representations of music are fractionated into subpopulations selective for different types of music, one of which is specialized for the analysis of song.

Selective responses to faces, scenes, and bodies in the ventral visual pathway of infants.

Three of the most robust functional landmarks in the human brain are the selective responses to faces in the fusiform face area (FFA), scenes in the parahippocampal place area (PPA), and bodies in the extrastriate body area (EBA). Are the selective responses of these regions present early in development or do they require many years to develop? Prior evidence leaves this question unresolved. We designed a new 32-channel infant magnetic resonance imaging (MRI) coil and collected high-quality functional MRI (fMRI) data from infants (2-9 months of age) while they viewed stimuli from four conditions-faces, bodies, objects, and scenes. We find that infants have face-, scene-, and body-selective responses in the location of the adult FFA, PPA, and EBA, respectively, powerfully constraining accounts of cortical development.

The neural architecture of language: Integrative modeling converges on predictive processing.

The neuroscience of perception has recently been revolutionized with an integrative modeling approach in which computation, brain function, and behavior are linked across many datasets and many computational models. By revealing trends across models, this approach yields novel insights into cognitive and neural mechanisms in the target domain. We here present a systematic study taking this approach to higher-level cognition: human language processing, our species' signature cognitive skill. We find that the most powerful "transformer" models predict nearly 100% of explainable variance in neural responses to sentences and generalize across different datasets and imaging modalities (functional MRI and electrocorticography). Models' neural fits ("brain score") and fits to behavioral responses are both strongly correlated with model accuracy on the next-word prediction task (but not other language tasks). Model architecture appears to substantially contribute to neural fit. These results provide computationally explicit evidence that predictive processing fundamentally shapes the language comprehension mechanisms in the human brain.

Computational models of category-selective brain regions enable high-throughput tests of selectivity.

Cortical regions apparently selective to faces, places, and bodies have provided important evidence for domain-specific theories of human cognition, development, and evolution. But claims of category selectivity are not quantitatively precise and remain vulnerable to empirical refutation. Here we develop artificial neural network-based encoding models that accurately predict the response to novel images in the fusiform face area, parahippocampal place area, and extrastriate body area, outperforming descriptive models and experts. We use these models to subject claims of category selectivity to strong tests, by screening for and synthesizing images predicted to produce high responses. We find that these high-response-predicted images are all unambiguous members of the hypothesized preferred category for each region. These results provide accurate, image-computable encoding models of each category-selective region, strengthen evidence for domain specificity in the brain, and point the way for future research characterizing the functional organization of the brain with unprecedented computational precision.

A size-adaptive 32-channel array coil for awake infant neuroimaging at 3 Tesla MRI.

PURPOSE: Functional magnetic resonance imaging (fMRI) during infancy poses challenges due to practical, methodological, and analytical considerations. The aim of this study was to implement a hardware-related approach to increase subject compliance for fMRI involving awake infants. To accomplish this, we designed, constructed, and evaluated an adaptive 32-channel array coil. METHODS: To allow imaging with a close-fitting head array coil for infants aged 1-18 months, an adjustable head coil concept was developed. The coil setup facilitates a half-seated scanning position to improve the infant's overall scan compliance. Earmuff compartments are integrated directly into the coil housing to enable the usage of sound protection without losing a snug fit of the coil around the infant's head. The constructed array coil was evaluated from phantom data using bench-level metrics, signal-to-noise ratio (SNR) performances, and accelerated imaging capabilities for both in-plane and simultaneous multislice (SMS) reconstruction methodologies. Furthermore, preliminary fMRI data were acquired to evaluate the in vivo coil performance. RESULTS: Phantom data showed a 2.7-fold SNR increase on average when compared with a commercially available 32-channel head coil. At the center and periphery regions of the infant head phantom, the SNR gains were measured to be 1.25-fold and 3-fold, respectively. The infant coil further showed favorable encoding capabilities for undersampled k-space reconstruction methods and SMS techniques. CONCLUSIONS: An infant-friendly head coil array was developed to improve sensitivity, spatial resolution, accelerated encoding, motion insensitivity, and subject tolerance in pediatric MRI. The adaptive 32-channel array coil is well-suited for fMRI acquisitions in awake infants.

Music-selective neural populations arise without musical training.

Recent work has shown that human auditory cortex contains neural populations anterior and posterior to primary auditory cortex that respond selectively to music. However, it is unknown how this selectivity for music arises. To test whether musical training is necessary, we measured fMRI responses to 192 natural sounds in 10 people with almost no musical training. When voxel responses were decomposed into underlying components, this group exhibited a music-selective component that was very similar in response profile and anatomical distribution to that previously seen in individuals with moderate musical training. We also found that musical genres that were less familiar to our participants (e.g., Balinese gamelan) produced strong responses within the music component, as did drum clips with rhythm but little melody, suggesting that these neural populations are broadly responsive to music as a whole. Our findings demonstrate that the signature properties of neural music selectivity do not require musical training to develop, showing that the music-selective neural populations are a fundamental and widespread property of the human brain.NEW & NOTEWORTHY We show that music-selective neural populations are clearly present in people without musical training, demonstrating that they are a fundamental and widespread property of the human brain. Additionally, we show music-selective neural populations respond strongly to music from unfamiliar genres as well as music with rhythm but little pitch information, suggesting that they are broadly responsive to music as a whole.

The Language Network Is Recruited but Not Required for Nonverbal Event Semantics.

The ability to combine individual concepts of objects, properties, and actions into complex representations of the world is often associated with language. Yet combinatorial event-level representations can also be constructed from nonverbal input, such as visual scenes. Here, we test whether the language network in the human brain is involved in and necessary for semantic processing of events presented nonverbally. In Experiment 1, we scanned participants with fMRI while they performed a semantic plausibility judgment task versus a difficult perceptual control task on sentences and line drawings that describe/depict simple agent-patient interactions. We found that the language network responded robustly during the semantic task performed on both sentences and pictures (although its response to sentences was stronger). Thus, language regions in healthy adults are engaged during a semantic task performed on pictorial depictions of events. But is this engagement necessary? In Experiment 2, we tested two individuals with global aphasia, who have sustained massive damage to perisylvian language areas and display severe language difficulties, against a group of age-matched control participants. Individuals with aphasia were severely impaired on the task of matching sentences to pictures. However, they performed close to controls in assessing the plausibility of pictorial depictions of agent-patient interactions. Overall, our results indicate that the left frontotemporal language network is recruited but not necessary for semantic processing of nonverbally presented events.