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Forseth, K. J.

Publications and source records attributed to Forseth, K. J..

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Supplementary motor area in speech initiation: a large-scale intracranial EEG evaluation of stereotyped word articulation

Speech production is known to engage a distributed network. The brain regions responsible for the initiation of articulation are unclear, and they would be expected to coordinate a distributed network. Using direct intracranial recordings in a large cohort, during stereotyped speech production to eliminate confounds of phonological and semantic complexity, we performed a comprehensive analysis of cortical sites engaged in speech initiation. We found that the supplementary motor area (SMA) was the earliest speech motor region to be active prior to speech onset and was active almost exclusively prior to articulation. Broadband gamma activity in the SMA was predictive of the response time of word production, predicting response time from 250 ms after stimulus onset. Neural activity in SMA began at a highly predictable time after stimulus onset and extended until speech onset. SMA activity offset coincided with ventral premotor cortex and primary motor activity onset. This suggests that the SMA may coordinate the concerted activation of motor execution cortex. Our results support the idea that SMA is a key node in the speech initiation network. Significance statementProducing speech requires coordination across multiple brain regions. One cortical region - the supplementary motor area (SMA) - has long been a candidate region to coordinate across other regions to initiate speech production. In this study, we used human intracranial recordings from patients with epilepsy to investigate the role of the SMA in initiating speech. In a picture-naming task, subjects repeated the word "scrambled" scores of times; using this condition to eliminate any linguistic confounds, we found that the SMA was consistently one of the earliest regions to activate during word production. We also uncovered the SMAs temporally precise tuning to speech onset at the single-trial level.

neuroscience↗

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↗

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↗

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↗

What The Brain Does As We Speak

AO_SCPLOWBSTRACTC_SCPLOWLanguage is a defining human behavior and is dependent on networks interactions amongst broadly distributed neuronal substrates. Transient dynamics between language regions that underpin speech production have long been postulated, yet have proven challenging to evaluate empirically. We used direct intracranial recordings during single word production to create a finely resolved spatiotemporal atlas (134 patients, 25810 electrodes, 40278 words) of the entire language-dominant cortex and used this to derive single-trial state-space sequences of network motifs. We derived 5 discrete neural states during the production of each word, distinguished by unique patterns of distributed cortical interaction. This interactive model was significantly better than a model of the same design but lacking interactions between regions in explaining observed activity. Our results eschew strict functional attribution to localized cortical populations, supporting instead the idea that cognitive processes are better explained by distributed metastable network states.

neuroscience↗

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↗

Dynamic brain interactions during picture naming

Brain computations involve multiple processes by which sensory information is encoded and transformed to drive behavior. These computations are thought to be mediated by dynamic interactions between populations of neurons. Here we demonstrate that human brains exhibit a reliable sequence of neural interactions during speech production. We use an autoregressive hidden Markov model to identify dynamical network states exhibited by electrocorticographic signals recorded from human neurosurgical patients. Our method resolves dynamic latent network states on a trial-by-trial basis. We characterize individual network states according to the patterns of directional information flow between cortical regions of interest. These network states occur consistently and in a specific, interpretable sequence across trials and subjects: a fixed-length visual processing state is followed by a variable-length language state, and then by a terminal articulation state. This empirical evidence validates classical psycholinguistic theories that have posited such intermediate states during speaking. It further reveals these state dynamics are not localized to one brain area or one sequence of areas, but are instead a network phenomenon.

neuroscience↗

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↗