Semantic Representations during Language Comprehension Are Affected by Context.

The meaning of words in natural language depends crucially on context. However, most neuroimaging studies of word meaning use isolated words and isolated sentences with little context. Because the brain may process natural language differently from how it processes simplified stimuli, there is a pressing need to determine whether prior results on word meaning generalize to natural language. fMRI was used to record human brain activity while four subjects (two female) read words in four conditions that vary in context: narratives, isolated sentences, blocks of semantically similar words, and isolated words. We then compared the signal-to-noise ratio (SNR) of evoked brain responses, and we used a voxelwise encoding modeling approach to compare the representation of semantic information across the four conditions. We find four consistent effects of varying context. First, stimuli with more context evoke brain responses with higher SNR across bilateral visual, temporal, parietal, and prefrontal cortices compared with stimuli with little context. Second, increasing context increases the representation of semantic information across bilateral temporal, parietal, and prefrontal cortices at the group level. In individual subjects, only natural language stimuli consistently evoke widespread representation of semantic information. Third, context affects voxel semantic tuning. Finally, models estimated using stimuli with little context do not generalize well to natural language. These results show that context has large effects on the quality of neuroimaging data and on the representation of meaning in the brain. Thus, neuroimaging studies that use stimuli with little context may not generalize well to the natural regime.SIGNIFICANCE STATEMENT Context is an important part of understanding the meaning of natural language, but most neuroimaging studies of meaning use isolated words and isolated sentences with little context. Here, we examined whether the results of neuroimaging studies that use out-of-context stimuli generalize to natural language. We find that increasing context improves the quality of neuro-imaging data and changes where and how semantic information is represented in the brain. These results suggest that findings from studies using out-of-context stimuli may not generalize to natural language used in daily life.

Task-Dependent Warping of Semantic Representations During Search for Visual Action Categories.

Object and action perception in cluttered dynamic natural scenes relies on efficient allocation of limited brain resources to prioritize the attended targets over distractors. It has been suggested that during visual search for objects, distributed semantic representation of hundreds of object categories is warped to expand the representation of targets. Yet, little is known about whether and where in the brain visual search for action categories modulates semantic representations. To address this fundamental question, we studied brain activity recorded from five subjects (1 female) via functional magnetic resonance imaging while they viewed natural movies and searched for either communication or locomotion actions. We find that attention directed to action categories elicits tuning shifts that warp semantic representations broadly across neocortex, and that these shifts interact with intrinsic selectivity of cortical voxels for target actions. These results suggest that attention serves to facilitate task performance during social interactions by dynamically shifting semantic selectivity towards target actions, and that tuning shifts are a general feature of conceptual representations in the brain.SIGNIFICANCE STATEMENTThe ability to swiftly perceive the actions and intentions of others is a crucial skill for humans, which relies on efficient allocation of limited brain resources to prioritise the attended targets over distractors. However, little is known about the nature of high-level semantic representations during natural visual search for action categories. Here we provide the first evidence showing that attention significantly warps semantic representations by inducing tuning shifts in single cortical voxels, broadly spread across occipitotemporal, parietal, prefrontal, and cingulate cortices. This dynamic attentional mechanism can facilitate action perception by efficiently allocating neural resources to accentuate the representation of task-relevant action categories.

Feature-space selection with banded ridge regression.

Encoding models provide a powerful framework to identify the information represented in brain recordings. In this framework, a stimulus representation is expressed within a feature space and is used in a regularized linear regression to predict brain activity. To account for a potential complementarity of different feature spaces, a joint model is fit on multiple feature spaces simultaneously. To adapt regularization strength to each feature space, ridge regression is extended to banded ridge regression, which optimizes a different regularization hyperparameter per feature space. The present paper proposes a method to decompose over feature spaces the variance explained by a banded ridge regression model. It also describes how banded ridge regression performs a feature-space selection, effectively ignoring non-predictive and redundant feature spaces. This feature-space selection leads to better prediction accuracy and to better interpretability. Banded ridge regression is then mathematically linked to a number of other regression methods with similar feature-space selection mechanisms. Finally, several methods are proposed to address the computational challenge of fitting banded ridge regressions on large numbers of voxels and feature spaces. All implementations are released in an open-source Python package called Himalaya.

Natural speech reveals the semantic maps that tile human cerebral cortex.

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 modelling of functional MRI (fMRI) data collected while subjects listened to hours of narrative stories. We show that the semantic system is organized into intricate patterns that seem to be 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.

The Representation of Semantic Information Across Human Cerebral Cortex During Listening Versus Reading Is Invariant to Stimulus Modality.

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.SIGNIFICANCE STATEMENT Humans can comprehend the meaning of words from both spoken and written language. It is therefore important to understand the relationship between the brain representations of spoken or written text. Here, we show that although the representation of semantic information in the human brain is quite complex, the semantic representations evoked by listening versus reading are almost identical. These results suggest that the representation of language semantics is independent of the sensory modality through which the semantic information is received.

Voxelwise encoding models with non-spherical multivariate normal priors.

Predictive models for neural or fMRI data are often fit using regression methods that employ priors on the model parameters. One widely used method is ridge regression, which employs a spherical multivariate normal prior that assumes equal and independent variance for all parameters. However, a spherical prior is not always optimal or appropriate. There are many cases where expert knowledge or hypotheses about the structure of the model parameters could be used to construct a better prior. In these cases, non-spherical multivariate normal priors can be employed using a generalized form of ridge known as Tikhonov regression. Yet Tikhonov regression is only rarely used in neuroscience. In this paper we discuss the theoretical basis for Tikhonov regression, demonstrate a computationally efficient method for its application, and show several examples of how Tikhonov regression can improve predictive models for fMRI data. We also show that many earlier studies have implicitly used Tikhonov regression by linearly transforming the regressors before performing ridge regression.

The Hierarchical Cortical Organization of Human Speech Processing.

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.SIGNIFICANCE STATEMENT To investigate the processing steps performed by the human brain to transform natural speech sound into meaningful language, we used models based on a hierarchical set of speech features to predict BOLD responses of individual voxels recorded in an fMRI experiment while subjects listened to natural speech. Both cerebral hemispheres were actively involved in speech processing in large and equal amounts. Also, the transformation from spectral features to semantic elements occurs early in the cortical speech-processing stream. Our experimental and analytical approaches are important alternatives and complements to standard approaches that use segmented speech and block designs, which report more laterality in speech processing and associated semantic processing to higher levels of cortex than reported here.

Functional Subdomains within Scene-Selective Cortex: Parahippocampal Place Area, Retrosplenial Complex, and Occipital Place Area.

Functional MRI studies suggest that at least three brain regions in human visual cortex-the parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area (OPA; often called the transverse occipital sulcus)-represent large-scale information in natural scenes. Tuning of voxels within each region is often assumed to be functionally homogeneous. To test this assumption, we recorded blood oxygenation level-dependent responses during passive viewing of complex natural movies. We then used a voxelwise modeling framework to estimate voxelwise category tuning profiles within each scene-selective region. In all three regions, cluster analysis of the voxelwise tuning profiles reveals two functional subdomains that differ primarily in their responses to animals, man-made objects, social communication, and movement. Thus, the conventional functional definitions of the PPA, RSC, and OPA appear to be too coarse. One attractive hypothesis is that this consistent functional subdivision of scene-selective regions is a reflection of an underlying anatomical organization into two separate processing streams, one selectively biased toward static stimuli and one biased toward dynamic stimuli. SIGNIFICANCE STATEMENT: Visual scene perception is a critical ability to survive in the real world. It is therefore reasonable to assume that the human brain contains neural circuitry selective for visual scenes. Here we show that responses in three scene-selective areas-identified in previous studies-carry information about many object and action categories encountered in daily life. We identify two subregions in each area: one that is selective for categories of man-made objects, and another that is selective for vehicles and locomotion-related action categories that appear in dynamic scenes. This consistent functional subdivision may reflect an anatomical organization into two processing streams, one biased toward static stimuli and one biased toward dynamic stimuli.

Eye movement-invariant representations in the human visual system.

During natural vision, humans make frequent eye movements but perceive a stable visual world. It is therefore likely that the human visual system contains representations of the visual world that are invariant to eye movements. Here we present an experiment designed to identify visual areas that might contain eye-movement-invariant representations. We used functional MRI to record brain activity from four human subjects who watched natural movies. In one condition subjects were required to fixate steadily, and in the other they were allowed to freely make voluntary eye movements. The movies used in each condition were identical. We reasoned that the brain activity recorded in a visual area that is invariant to eye movement should be similar under fixation and free viewing conditions. In contrast, activity in a visual area that is sensitive to eye movement should differ between fixation and free viewing. We therefore measured the similarity of brain activity across repeated presentations of the same movie within the fixation condition, and separately between the fixation and free viewing conditions. The ratio of these measures was used to determine which brain areas are most likely to contain eye movement-invariant representations. We found that voxels located in early visual areas are strongly affected by eye movements, while voxels in ventral temporal areas are only weakly affected by eye movements. These results suggest that the ventral temporal visual areas contain a stable representation of the visual world that is invariant to eye movements made during natural vision.

A voxel-wise encoding model for early visual areas decodes mental images of remembered scenes.

Recent multi-voxel pattern classification (MVPC) studies have shown that in early visual cortex patterns of brain activity generated during mental imagery are similar to patterns of activity generated during perception. This finding implies that low-level visual features (e.g., space, spatial frequency, and orientation) are encoded during mental imagery. However, the specific hypothesis that low-level visual features are encoded during mental imagery is difficult to directly test using MVPC. The difficulty is especially acute when considering the representation of complex, multi-object scenes that can evoke multiple sources of variation that are distinct from low-level visual features. Therefore, we used a voxel-wise modeling and decoding approach to directly test the hypothesis that low-level visual features are encoded in activity generated during mental imagery of complex scenes. Using fMRI measurements of cortical activity evoked by viewing photographs, we constructed voxel-wise encoding models of tuning to low-level visual features. We also measured activity as subjects imagined previously memorized works of art. We then used the encoding models to determine if putative low-level visual features encoded in this activity could pick out the imagined artwork from among thousands of other randomly selected images. We show that mental images can be accurately identified in this way; moreover, mental image identification accuracy depends upon the degree of tuning to low-level visual features in the voxels selected for decoding. These results directly confirm the hypothesis that low-level visual features are encoded during mental imagery of complex scenes. Our work also points to novel forms of brain-machine interaction: we provide a proof-of-concept demonstration of an internet image search guided by mental imagery.

Functional subdomains within human FFA.

The fusiform face area (FFA) is a well-studied human brain region that shows strong activation for faces. In functional MRI studies, FFA is often assumed to be a homogeneous collection of voxels with similar visual tuning. To test this assumption, we used natural movies and a quantitative voxelwise modeling and decoding framework to estimate category tuning profiles for individual voxels within FFA. We find that the responses in most FFA voxels are strongly enhanced by faces, as reported in previous studies. However, we also find that responses of individual voxels are selectively enhanced or suppressed by a wide variety of other categories and that these broader tuning profiles differ across FFA voxels. Cluster analysis of category tuning profiles across voxels reveals three spatially segregated functional subdomains within FFA. These subdomains differ primarily in their responses for nonface categories, such as animals, vehicles, and communication verbs. Furthermore, this segregation does not depend on the statistical threshold used to define FFA from responses to functional localizers. These results suggest that voxels within FFA represent more diverse information about object and action categories than generally assumed.

Identifying natural images from human brain activity.

A challenging goal in neuroscience is to be able to read out, or decode, mental content from brain activity. Recent functional magnetic resonance imaging (fMRI) studies have decoded orientation, position and object category from activity in visual cortex. However, these studies typically used relatively simple stimuli (for example, gratings) or images drawn from fixed categories (for example, faces, houses), and decoding was based on previous measurements of brain activity evoked by those same stimuli or categories. To overcome these limitations, here we develop a decoding method based on quantitative receptive-field models that characterize the relationship between visual stimuli and fMRI activity in early visual areas. These models describe the tuning of individual voxels for space, orientation and spatial frequency, and are estimated directly from responses evoked by natural images. We show that these receptive-field models make it possible to identify, from a large set of completely novel natural images, which specific image was seen by an observer. Identification is not a mere consequence of the retinotopic organization of visual areas; simpler receptive-field models that describe only spatial tuning yield much poorer identification performance. Our results suggest that it may soon be possible to reconstruct a picture of a person's visual experience from measurements of brain activity alone.

The cortical representation of language timescales is shared between reading and listening.

Language comprehension involves integrating low-level sensory inputs into a hierarchy of increasingly high-level features. Prior work studied brain representations of different levels of the language hierarchy, but has not determined whether these brain representations are shared between written and spoken language. To address this issue, we analyze fMRI BOLD data that were recorded while participants read and listened to the same narratives in each modality. Levels of the language hierarchy are operationalized as timescales, where each timescale refers to a set of spectral components of a language stimulus. Voxelwise encoding models are used to determine where different timescales are represented across the cerebral cortex, for each modality separately. These models reveal that between the two modalities timescale representations are organized similarly across the cortical surface. Our results suggest that, after low-level sensory processing, language integration proceeds similarly regardless of stimulus modality.

Occipital-temporal cortical tuning to semantic and affective features of natural images predicts associated behavioral responses.

In everyday life, people need to respond appropriately to many types of emotional stimuli. Here, we investigate whether human occipital-temporal cortex (OTC) shows co-representation of the semantic category and affective content of visual stimuli. We also explore whether OTC transformation of semantic and affective features extracts information of value for guiding behavior. Participants viewed 1620 emotional natural images while functional magnetic resonance imaging data were acquired. Using voxel-wise modeling we show widespread tuning to semantic and affective image features across OTC. The top three principal components underlying OTC voxel-wise responses to image features encoded stimulus animacy, stimulus arousal and interactions of animacy with stimulus valence and arousal. At low to moderate dimensionality, OTC tuning patterns predicted behavioral responses linked to each image better than regressors directly based on image features. This is consistent with OTC representing stimulus semantic category and affective content in a manner suited to guiding behavior.

The Cortical Representation of Language Timescales is Shared between Reading and Listening.

Language comprehension involves integrating low-level sensory inputs into a hierarchy of increasingly high-level features. Prior work studied brain representations of different levels of the language hierarchy, but has not determined whether these brain representations are shared between written and spoken language. To address this issue, we analyzed fMRI BOLD data recorded while participants read and listened to the same narratives in each modality. Levels of the language hierarchy were operationalized as timescales, where each timescale refers to a set of spectral components of a language stimulus. Voxelwise encoding models were used to determine where different timescales are represented across the cerebral cortex, for each modality separately. These models reveal that between the two modalities timescale representations are organized similarly across the cortical surface. Our results suggest that, after low-level sensory processing, language integration proceeds similarly regardless of stimulus modality.

Model connectivity: leveraging the power of encoding models to overcome the limitations of functional connectivity.

Functional connectivity (FC) is the most popular method for recovering functional networks of brain areas with fMRI. However, because FC is defined as temporal correlations in brain activity, FC networks are confounded by noise and lack a precise functional role. To overcome these limitations, we developed model connectivity (MC). MC is defined as similarities in encoding model weights, which quantify reliable functional activity in terms of interpretable stimulus- or task-related features. To compare FC and MC, both methods were applied to a naturalistic story listening dataset. FC recovered spatially broad networks that are confounded by noise, and that lack a clear role during natural language comprehension. By contrast, MC recovered spatially localized networks that are robust to noise, and that represent distinct categories of semantic concepts. Thus, MC is a powerful data-driven approach for recovering and interpreting the functional networks that support complex cognitive processes.

Phonemic segmentation of narrative speech in human cerebral cortex.

Speech processing requires extracting meaning from acoustic patterns using a set of intermediate representations based on a dynamic segmentation of the speech stream. Using whole brain mapping obtained in fMRI, we investigate the locus of cortical phonemic processing not only for single phonemes but also for short combinations made of diphones and triphones. We find that phonemic processing areas are much larger than previously described: they include not only the classical areas in the dorsal superior temporal gyrus but also a larger region in the lateral temporal cortex where diphone features are best represented. These identified phonemic regions overlap with the lexical retrieval region, but we show that short word retrieval is not sufficient to explain the observed responses to diphones. Behavioral studies have shown that phonemic processing and lexical retrieval are intertwined. Here, we also have identified candidate regions within the speech cortical network where this joint processing occurs.

Bringing the Clinic Home: An At-Home Multi-Modal Data Collection Ecosystem to Support Adaptive Deep Brain Stimulation.

Adaptive deep brain stimulation (aDBS) shows promise for improving treatment for neurological disorders such as Parkinson's disease (PD). aDBS uses symptom-related biomarkers to adjust stimulation parameters in real-time to target symptoms more precisely. To enable these dynamic adjustments, parameters for an aDBS algorithm must be determined for each individual patient. This requires time-consuming manual tuning by clinical researchers, making it difficult to find an optimal configuration for a single patient or to scale to many patients. Furthermore, the long-term effectiveness of aDBS algorithms configured in-clinic while the patient is at home remains an open question. To implement this therapy at large scale, a methodology to automatically configure aDBS algorithm parameters while remotely monitoring therapy outcomes is needed. In this paper, we share a design for an at-home data collection platform to help the field address both issues. The platform is composed of an integrated hardware and software ecosystem that is open-source and allows for at-home collection of neural, inertial, and multi-camera video data. To ensure privacy for patient-identifiable data, the platform encrypts and transfers data through a virtual private network. The methods include time-aligning data streams and extracting pose estimates from video recordings. To demonstrate the use of this system, we deployed this platform to the home of an individual with PD and collected data during self-guided clinical tasks and periods of free behavior over the course of 1.5 years. Data were recorded at sub-therapeutic, therapeutic, and supra-therapeutic stimulation amplitudes to evaluate motor symptom severity under different therapeutic conditions. These time-aligned data show the platform is capable of synchronized at-home multi-modal data collection for therapeutic evaluation. This system architecture may be used to support automated aDBS research, to collect new datasets and to study the long-term effects of DBS therapy outside the clinic for those suffering from neurological disorders.

A three-dimensional spatiotemporal receptive field model explains responses of area MT neurons to naturalistic movies.

Area MT has been an important target for studies of motion processing. However, previous neurophysiological studies of MT have used simple stimuli that do not contain many of the motion signals that occur during natural vision. In this study we sought to determine whether views of area MT neurons developed using simple stimuli can account for MT responses under more naturalistic conditions. We recorded responses from macaque area MT neurons during stimulation with naturalistic movies. We then used a quantitative modeling framework to discover which specific mechanisms best predict neuronal responses under these challenging conditions. We find that the simplest model that accurately predicts responses of MT neurons consists of a bank of V1-like filters, each followed by a compressive nonlinearity, a divisive nonlinearity, and linear pooling. Inspection of the fit models shows that the excitatory receptive fields of MT neurons tend to lie on a single plane within the three-dimensional spatiotemporal frequency domain, and suppressive receptive fields lie off this plane. However, most excitatory receptive fields form a partial ring in the plane and avoid low temporal frequencies. This receptive field organization ensures that most MT neurons are tuned for velocity but do not tend to respond to ambiguous static textures that are aligned with the direction of motion. In sum, MT responses to naturalistic movies are largely consistent with predictions based on simple stimuli. However, models fit using naturalistic stimuli reveal several novel properties of MT receptive fields that had not been shown in prior experiments.