Biology subjects

Rollo, P. S.

Publications and source records attributed to Rollo, P. S..

7 recordsLinked to original sources

bioRxiv2022

The spatiotemporal dynamics of semantic integration in the human brain

Language depends critically on the integration of lexical information to derive semantic concepts. The neurobiology of this fundamental aspect of human cognition remains mostly unknown. Limitations of spatiotemporal resolution have previously rendered it difficult to disentangle processes involved in semantic integration from independent computations such as tracking word meaning and establishing referents. We utilized intracranial recordings (n = 58) during the presentation of orthographic descriptions that were either referential or non-referential to a common object. Referential contexts enabled high frequency broadband gamma activation (70-150 Hz) of a distributed network including the inferior frontal sulcus (IFS), medial parietal cortex (MPC) and medial temporal lobe (MTL) in the left, language-dominant hemisphere. Components of this network (IFS, MPC), alongside posterior superior temporal sulcus, showed greater engagement for trials that did not progressively isolate a limited set of referents, relative to trials that did. IFS and posterior middle temporal gyrus activity was modulated by semantic coherence, regardless of whether the sentence picked out a common object. Centered around IFS and spreading out dorsally towards middle frontal gyrus and ventrally towards anterior/posterior inferior frontal gyrus, we uncovered a cortical mosaic of functional specialization for reference, coherence and semantic narrowing. Early processing windows implicated IFS in all aspects of semantics, and in later windows sub-portions of IFS exposed a clearer functional tessellation with some remaining overlap. This work unveils how lateral fronto-temporal regions make distinctly rich semantic contributions and are involved jointly in semantic integration and conflict resolution, depending on the sub-region and processing stage.

neuroscience↗

bioRxiv2021

The critical role of the ventral temporal lobe in word retrieval

Deficits in word retrieval are a hallmark of a variety of neurological illnesses spanning from dementia to traumatic injuries. The role of the dominant temporal lobe in fluent naming has been characterized by lesional analyses, functional imaging, and intracranial recordings, but limitations of each of these measures preclude a clear assessment of which specific constituent of the temporal lobe is critical for naming. We studied a large cohort of patients undergoing surgical resections or laser ablations of the dominant temporal lobe for medically intractable epilepsy (n=95). These techniques are exceedingly effective for seizure control but often result in language declines, particularly in confrontation naming, which can be socio-economically disabling. We used a multivariate voxel-based lesion symptom mapping analysis to localize brain regions significantly associated with visual object naming deficits. We observed that posterior inferior temporal regions, centered around the middle fusiform gyrus, were significantly associated with a decline in confrontation naming. Furthermore, we found that the posterior margin of anterior temporal lobectomies was linearly correlated to a decline in visual naming with a clinically significant decline occurring once the resection extended 6 cm from the anterior tip of the temporal lobe. We integrated these findings with electrocorticography during naming in a subset of this population and found that the majority of cortical regions whose resection was associated with a significant decline overlapped with regions that were functionally most active prior to articulation. Importantly, these loci coincide with the sites of susceptibility artifacts during echo-planar imaging, which explains why this region has not previously been implicated. Taken together, these data highlight the crucial contribution of the posterior ventral temporal cortex in lexical access and its important role in the pathophysiology of anomia following temporal lobe resections. Surgical strategies, including the use of laser ablation to target the medial temporal lobe as well as microsurgical approaches, should attempt to preserve this region to mitigate postoperative language deficits.

neuroscience↗

bioRxiv2021

Event-Related Phase Synchronization Propagates Rapidly across Human VentralVisual 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.

neuroscience↗

bioRxiv2021

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 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 gamma 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 dual-route models of reading, with parallel processes via the lexical route from mFus to IFG, and the sub-lexical route from IPS and precentral sulcus to anterior IFG.

neuroscience↗

bioRxiv2021

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, 19 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 in 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 (approximately 300-700 ms), and these were localized to neighboring electrodes in pSTS. The pars triangularis and temporal pole encode anticipation of composition in broadband low frequencies, and both regions exhibit greater functional connectivity with pSTS during phrase composition. Our results suggest that the pSTS is a highly specialized region comprised 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. SignificanceLinguists 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.

neuroscience↗

bioRxiv2020

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. However, the neural constituents and their interactions that allow us to identify written words are not well understood. Using direct intracranial recordings in a large cohort of humans, we comprehensively isolated the spatiotemporal dynamics of visual word recognition across the entire left ventral occipitotemporal cortex. The mid-fusiform cortex is the first region that is sensitive to word identity and to both sub-lexical and lexical frequencies. Its activation, response latency and amplitude, are highly dependent on the statistics of natural language. Information about lexicality and word frequency propagates posteriorly from this region to traditional visual word form regions and to earlier visual cortex. This unique sensitivity of mid-fusiform cortex to the lexical characteristics of written words points to its central role as an orthographic lexicon, which accesses the long-term memory representations of visual word forms.

neuroscience↗

bioRxiv2018

Prediction in Human Auditory Cortex

Spoken language is thought to be facilitated by an ensemble of predictive mechanisms, yet the neurobiology of prediction for both speech perception and production remains unknown. We used intracranial recordings (31 patients, 6580 electrodes) from depth probes implanted along the anteroposterior extent of the supratemporal plane during rhythm listening, speech perception, and speech production. This revealed a frequency-multiplexed encoding of sublexical features during entrainment and a traveling wave of high-frequency activity across Heschls gyrus. Critically, we isolated two predictive mechanisms in early auditory cortex with distinct anatomical and functional characteristics. The first mechanism, localized to bilateral Heschls gyrus and indexed by low-frequency phase, predicts the timing of acoustic events (\"when\"). The second mechanism, localized to planum temporale in the language-dominant hemisphere and indexed by gamma power, predicts the acoustic consequence of speech motor plans (\"what\"). This work grounds cognitive models of speech perception and production in human neurobiology, illuminating the fundamental acoustic infrastructure - both architecture and function - for spoken language.

neuroscience↗