The spatiotemporal dynamics of semantic integration in the human brain.

Language depends critically on the integration of lexical information across multiple words to derive semantic concepts. Limitations of spatiotemporal resolution have previously rendered it difficult to isolate processes involved in semantic integration. We utilized intracranial recordings in epilepsy patients (n = 58) who read written word definitions. Descriptions were either referential or non-referential to a common object. Semantically referential sentences enabled high frequency broadband gamma activation (70-150 Hz) of the inferior frontal sulcus (IFS), medial parietal cortex, orbitofrontal cortex (OFC) and medial temporal lobe in the left, language-dominant hemisphere. IFS, OFC and posterior middle temporal gyrus activity was modulated by the semantic coherence of non-referential sentences, exposing semantic effects that were independent of task-based referential status. Components of this network, alongside posterior superior temporal sulcus, were engaged for referential sentences that did not clearly reduce the lexical search space by the final word. These results indicate the existence of complementary cortical mosaics for semantic integration in posterior temporal and inferior frontal cortex.

Spatiotemporally distributed frontotemporal networks for sentence reading.

Reading a sentence entails integrating the meanings of individual words to infer more complex, higher-order meaning. This highly rapid and complex human behavior is known to engage the inferior frontal gyrus (IFG) and middle temporal gyrus (MTG) in the language-dominant hemisphere, yet whether there are distinct contributions of these regions to sentence reading is still unclear. To probe these neural spatiotemporal dynamics, we used direct intracranial recordings to measure neural activity while reading sentences, meaning-deficient Jabberwocky sentences, and lists of words or pseudowords. We isolated two functionally and spatiotemporally distinct frontotemporal networks, each sensitive to distinct aspects of word and sentence composition. The first distributed network engages the IFG and MTG, with IFG activity preceding MTG. Activity in this network ramps up over the duration of a sentence and is reduced or absent during Jabberwocky and word lists, implying its role in the derivation of sentence-level meaning. The second network engages the superior temporal gyrus and the IFG, with temporal responses leading those in frontal lobe, and shows greater activation for each word in a list than those in sentences, suggesting that sentential context enables greater efficiency in the lexical and/or phonological processing of individual words. These adjacent, yet spatiotemporally dissociable neural mechanisms for word- and sentence-level processes shed light on the richly layered semantic networks that enable us to fluently read. These results imply distributed, dynamic computation across the frontotemporal language network rather than a clear dichotomy between the contributions of frontal and temporal structures.

Critical role of the ventral temporal lobe in naming.

OBJECTIVE: Lexical retrieval deficits are characteristic of a variety of different neurological disorders. However, the exact substrates responsible for this are not known. We studied a large cohort of patients undergoing surgery in the dominant temporal lobe for medically intractable epilepsy (n = 95) to localize brain regions that were associated with anomia. METHODS: We performed a multivariate voxel-based lesion-symptom mapping analysis to correlate surgical lesions within the temporal lobe with changes in naming ability. Additionally, we used a surface-based mixed-effects multilevel analysis to estimate group-level broadband gamma activity during naming across a subset of patients with electrocorticographic recordings and integrated these results with lesion-deficit findings. RESULTS: We observed that ventral temporal regions, centered around the middle fusiform gyrus, were significantly associated with a decline in naming. Furthermore, we found that the ventral aspect of temporal lobectomies was linearly correlated to a decline in naming, with a clinically significant decline occurring once the resection extended 6 cm from the anterior tip of the temporal lobe on the ventral surface. On electrocorticography, the majority of these cortical regions were functionally active following visual processing. These loci coincide with the sites of susceptibility artifacts during echoplanar imaging, which may explain why this region has been previously underappreciated as the locus responsible for postoperative naming deficits. SIGNIFICANCE: Taken together, these data highlight the crucial contribution of the ventral temporal cortex in naming and its important role in the pathophysiology of anomia following temporal lobe resections. As such, surgical strategies should attempt to preserve this region to mitigate postoperative language deficits.

Event-related phase synchronization propagates rapidly across human ventral visual cortex.

Visual inputs to early visual cortex integrate with semantic, linguistic and memory inputs in higher visual cortex, in a manner that is rapid and accurate, and enables complex computations such as face recognition and word reading. This implies the existence of fundamental organizational principles that enable such efficiency. To elaborate on this, we performed intracranial recordings in 82 individuals while they performed tasks of varying visual and cognitive complexity. We discovered that visual inputs induce highly organized posterior-to-anterior propagating patterns of phase modulation across the ventral occipitotemporal cortex. At individual electrodes there was a stereotyped temporal pattern of phase progression following both stimulus onset and offset, consistent across trials and tasks. The phase of low frequency activity in anterior regions was predicted by the prior phase in posterior cortical regions. This spatiotemporal propagation of phase likely serves as a feed-forward organizational influence enabling the integration of information across the ventral visual stream. This phase modulation manifests as the early components of the event related potential; one of the most commonly used measures in human electrophysiology. These findings illuminate fundamental organizational principles of the higher order visual system that enable the rapid recognition and characterization of a variety of inputs.

A Spatiotemporal Map of Reading Aloud.

Reading words aloud is a fundamental aspect of literacy. The rapid rate at which multiple distributed neural substrates are engaged in this process can only be probed via techniques with high spatiotemporal resolution. We probed this with direct intracranial recordings covering most of the left hemisphere in 46 humans (26 male, 20 female) as they read aloud regular, exception and pseudo-words. We used this to create a spatiotemporal map of word processing and to derive how broadband γ activity varies with multiple word attributes critical to reading speed: lexicality, word frequency, and orthographic neighborhood. We found that lexicality is encoded earliest in mid-fusiform (mFus) cortex, and precentral sulcus, and is represented reliably enough to allow single-trial lexicality decoding. Word frequency is first represented in mFus and later in the inferior frontal gyrus (IFG) and inferior parietal sulcus (IPS), while orthographic neighborhood sensitivity resides solely in IPS. We thus isolate the neural correlates of the distributed reading network involving mFus, IFG, IPS, precentral sulcus, and motor cortex and provide direct evidence for parallel processes via the lexical route from mFus to IFG, and the sublexical route from IPS and precentral sulcus to anterior IFG.SIGNIFICANCE STATEMENT Reading aloud depends on multiple complex cerebral computations: mapping from a written letter string on a page to a sequence of spoken sound representations. Here, we used direct intracranial recordings in a large cohort while they read aloud known and novel words, to track, across space and time, the progression of neural representations of behaviorally relevant factors that govern reading speed. We find, concordant with cognitive models of reading, that known and novel words are differentially processed through a lexical route, sensitive to frequency of occurrence of known words in natural language, and a sublexical route, performing letter-by-letter construction of novel words.

Minimal Phrase Composition Revealed by Intracranial Recordings.

The ability to comprehend phrases is an essential integrative property of the brain. Here, we evaluate the neural processes that enable the transition from single-word processing to a minimal compositional scheme. Previous research has reported conflicting timing effects of composition, and disagreement persists with respect to inferior frontal and posterior temporal contributions. To address these issues, 19 patients (10 male, 9 female) implanted with penetrating depth or surface subdural intracranial electrodes, heard auditory recordings of adjective-noun, pseudoword-noun, and adjective-pseudoword phrases and judged whether the phrase matched a picture. Stimulus-dependent alterations in broadband gamma activity, low-frequency power, and phase-locking values across the language-dominant left hemisphere were derived. This revealed a mosaic located on the lower bank of the posterior superior temporal sulcus (pSTS), in which closely neighboring cortical sites displayed exclusive sensitivity to either lexicality or phrase structure, but not both. Distinct timings were found for effects of phrase composition (210-300 ms) and pseudoword processing (∼300-700 ms), and these were localized to neighboring electrodes in pSTS. The pars triangularis and temporal pole encoded anticipation of composition in broadband low frequencies, and both regions exhibited greater functional connectivity with pSTS during phrase composition. Our results suggest that the pSTS is a highly specialized region composed of sparsely interwoven heterogeneous constituents that encodes both lower and higher level linguistic features. This hub in pSTS for minimal phrase processing may form the neural basis for the human-specific computational capacity for forming hierarchically organized linguistic structures.SIGNIFICANCE STATEMENT Linguists have claimed that the integration of multiple words into a phrase demands a computational procedure distinct from single-word processing. Here, we provide intracranial recordings from a large patient cohort, with high spatiotemporal resolution, to track the cortical dynamics of phrase composition. Epileptic patients volunteered to participate in a task in which they listened to phrases (red boat), word-pseudoword or pseudoword-word pairs (e.g., red fulg). At the onset of the second word in phrases, greater broadband high gamma activity was found in posterior superior temporal sulcus in electrodes that exclusively indexed phrasal meaning and not lexical meaning. These results provide direct, high-resolution signatures of minimal phrase composition in humans, a potentially species-specific computational capacity.

Dataset of human intracranial recordings during famous landmark identification.

For most people, recalling information about familiar items in a visual scene is an effortless task, but it is one that depends on coordinated interactions of multiple, distributed neural components. We leveraged the high spatiotemporal resolution of direct intracranial recordings to better delineate the network dynamics underpinning visual scene recognition. We present a dataset of recordings from a large cohort of humans while they identified images of famous landmarks (50 individuals, 52 recording sessions, 6,775 electrodes, 6,541 trials). This dataset contains local field potential recordings derived from subdural and penetrating electrodes covering broad areas of cortex across both hemispheres. We provide this pre-processed data with behavioural metrics (correct/incorrect, response times) and electrode localisation in a population-normalised cortical surface space. This rich dataset will allow further investigation into the spatiotemporal progression of multiple neural processes underlying visual processing, scene recognition and cued memory recall.

Spatiotemporal dynamics of orthographic and lexical processing in the ventral visual pathway.

Reading is a rapid, distributed process that engages multiple components of the ventral visual stream. To understand the neural constituents and their interactions that allow us to identify written words, we performed direct intra-cranial recordings in a large cohort of humans. This allowed us to isolate the spatiotemporal dynamics of visual word recognition across the entire left ventral occipitotemporal cortex. We found that mid-fusiform cortex is the first brain region sensitive to lexicality, preceding the traditional visual word form area. The magnitude and duration of its activation are driven by the statistics of natural language. Information regarding lexicality and word frequency propagates posteriorly from this region to visual word form regions and to earlier visual cortex, which, while active earlier, show sensitivity to words later. Further, direct electrical stimulation of this region results in reading arrest, further illustrating its crucial role in reading. This unique sensitivity of mid-fusiform cortex to sub-lexical and lexical characteristics points to its central role as the orthographic lexicon-the long-term memory representations of visual word forms.

Oblique trajectory angles in robotic stereo-electroencephalography.

OBJECTIVE: Traditional stereo-electroencephalography (sEEG) entails the use of orthogonal trajectories guided by seizure semiology and arteriography. Advances in robotic stereotaxy and computerized neuronavigation have made oblique trajectories more feasible and easier to implement without formal arteriography. Such trajectories provide access to components of seizure networks not readily sampled using orthogonal trajectories. However, the dogma regarding the relative safety and predictability of orthogonal and azimuth-based trajectories persists, given the absence of data regarding the safety and efficacy of oblique sEEG trajectories. In this study, the authors evaluated the relative accuracy and efficacy of both orthogonal and oblique trajectories during robotic implantation of sEEG electrodes to sample seizure networks. METHODS: The authors performed a retrospective analysis of 150 consecutive procedures in 134 patients, accounting for 2040 electrode implantations. Of these, 837 (41%) were implanted via oblique trajectories (defined as an entry angle > 30°). Accuracy was calculated by comparing the deviation of each electrode at the entry and the target point from the planned trajectory using postimplantation imaging. RESULTS: The mean entry and target deviations were 1.57 mm and 1.89 mm for oblique trajectories compared with 1.38 mm and 1.69 mm for orthogonal trajectories, respectively. Entry point deviation was significantly associated with entry angle, but the impact of this relationship was negligible (-0.015-mm deviation per degree). Deviation at the target point was not significantly affected by the entry angle. No hemorrhagic or infectious complications were observed in the entire cohort, further suggesting that these differences were not meaningful in a clinical context. Of the patients who then underwent definitive procedures after sEEG, 69 patients had a minimum of 12 months of follow-up, of whom 58 (84%) achieved an Engel class I or II outcome during a median follow-up of 27 months. CONCLUSIONS: The magnitude of stereotactic errors in this study falls squarely within the range reported in the sEEG literature, which primarily features orthogonal trajectories. The patient outcomes reported in this study suggest that seizure foci are well localized using oblique trajectories. Thus, the selective use of oblique trajectories in the authors' cohort was associated with excellent safety and efficacy, with no patient incidents, and the findings support the use of oblique trajectories as an effective and safe means of investigating seizure networks.

Category Selectivity for Face and Scene Recognition in Human Medial Parietal Cortex.

The rapid recognition and memory of faces and scenes implies the engagement of category-specific computational hubs in the ventral visual stream with the distributed cortical memory network. To better understand how recognition and identification occur in humans, we performed direct intracranial recordings, in a large cohort of patients (n = 50), from the medial parietal cortex (MPC) and the medial temporal lobe (MTL), structures known to be engaged during face and scene identification. We discovered that the MPC is topologically tuned to face and scene recognition, with clusters in MPC performing scene recognition bilaterally and face recognition in right subparietal sulcus. The MTL displayed a selectivity gradient with anterior, entorhinal cortex showing face selectivity and posterior parahippocampal regions showing scene selectivity. In both MPC and MTL, stimulus-specific identifiable exemplars led to greater activity in these cortical patches. These two regions work in concert for recognition of faces and scenes. Feature selectivity and identity-sensitive activity in the two regions was coincident, and they exhibited theta-phase locking during face and scene recognition. These findings together provide clear evidence for a specific role of subregions in the MPC for the recognition of unique entities.