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Peelle, J. E.

Publications and source records attributed to Peelle, J. E..

11 recordsLinked to original sources

Naturalistic Movie Viewing Reveals a Distributed Network Supporting Audiovisual Speech Processing

Traditional paradigms in cognitive neuroscience often fail to capture the richness of real-world experiences. To bridge this gap, researchers increasingly use naturalistic stimuli such as movies, which provide complex, multisensory input. Speech perception is a prime example of such complexity: it is inherently multisensory, involving the integration of auditory cues, lip movements, and facial expressions. Prior studies suggest that the left posterior superior temporal sulcus (pSTS) and superior temporal gyrus (STG) play a critical role in this integration. However, most studies of audiovisual speech have relied on simplified or artificial stimuli, limiting ecological validity. To address these gaps, we analyzed fMRI data from human participants watching two full-length films (500 Days of Summer, Citizenfour) to assess the consistency of multisensory speech processes across distinct genres and narratives. We manually annotated word onset times and modality (audiovisual vs. auditory-only). Across two movies and 38 participants we observed consistent speech-related activation in the pSTS and STG across speech types. Compared to auditory-only speech, audiovisual speech recruited a broad left-lateralized network including the angular gyrus, posterior temporal cortex, temporal pole, and inferior frontal gyrus, along with the right cerebellum. These findings were also consistently present in single-subject data. Importantly, most of the regions observed in our analyses have been implicated in multisensory function in the nonhuman primate literature despite receiving relatively little focus in human neuroimaging. Together our results demonstrate that speech processing during naturalistic viewing recruits a distributed network extending substantially beyond regions traditionally emphasized in audiovisual speech research.

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Caudate dopamine predicts cognitive effort decisions both in the lab and daily life

Making choices about whether and when to engage cognitive effort is a common feature of human everyday experience with important consequences for academic, career, and health outcomes. Yet, despite its importance, little is understood about the neurochemical mechanisms that underlie individual differences in the willingness to engage in cognitively effortful activities. To examine this question, we employed a multi-modal neuroimaging approach in which participants performed the Cognitive Effort Discounting paradigm (Cog-ED) while simultaneous PET-fMRI was acquired. We assessed both individual differences in dopamine-D2 receptor availability and brain activity during decision-making. In addition, the same participants performed a parametric working memory task (N-Back) and reported the cognitive effort associated with their daily life activities through a seven-day Ecological Momentary Assessment (EMA) protocol. The findings suggest a central role for caudate dopamine-D2 receptors in modulating cognitive effort-related motivation. People with higher caudate dopamine-D2 receptor availability had better working memory function, heightened sensitivity to effort costs, and greater modulation of brain activity during effort valuation. These laboratory findings also translated directly to daily life: higher levels of caudate dopamine-D2 receptors were associated with greater engagement in cognitively effortful activities. Together, the results suggest that how individuals determine the motivational value of cognitively effortful activities strongly depends on the dopamine system.

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Neural tracking of surprisal and semantic distance in naturalistic movie viewing

Understanding speech requires listeners to integrate incoming input with prior linguistic and thematic knowledge to access meaning, a task greatly aided by prediction. Surprisal and related phenomena (e.g., next word prediction) tend to be associated with broad activation of language regions during listening. A major challenge for interpreting the neural correlates of surprisal is that lexical expectancies are constrained both by syntactic and semantic information. In contrast, semantic distance yields more of a pure metric of relatedness between one language constituent (e.g., word, phrase, n-gram) and another within a high-dimensional semantic space. We contrasted surprisal and semantic distance in running discourse during naturalistic audiovisual language comprehension. We analyzed fMRI scans from 20 English-speaking adults who viewed the full-length film 500 Days of Summer. Our focus was on brain sensitivity to either surprisal or semantic distance as language unfolded word-by-word. To this end, we implemented a series of hierarchical voxelwise encoding models. After accounting for low-level auditory and visual features, the addition of either surprisal or semantic distance improved prediction in bilateral superior temporal gyrus (STG), left inferior frontal gyrus, and right cerebellum. Critically, both semantic distance and surprisal explained unique variation in bilateral temporal cortex after accounting for the other. These results support the notion that the brain tracks both broad probabilistic prediction as well as semantic integration. More generally, these findings extend previous work on auditory-only speech by demonstrating that surprisal and semantic distance predict meaningful neural variation even within a rich audiovisual context.

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Multi-site MRI analysis of morphometric differences in brain regions in the presence of hearing loss and tinnitus across the adult lifespan

The impact of age and hearing loss on the brain has garnered significant attention, as both factors have been implicated in the development of cognitive impairment or dementia. In this study, we investigated the impact of hearing loss and tinnitus on gray matter in the brain, while accounting for age. We used a comprehensive secondary analysis of structural MRI data obtained from multiple research sites (256 unique individuals) using voxel-based and surface-based morphology. After harmonization of this multi-site brain data, our research replicated the previously reported finding of age-related decline in total cortical volume, but there was no significant effect of either hearing loss or tinnitus on total cortical volume. When a region of interest analysis was conducted, the hippocampus emerged as the only brain region that showed a direct impact of hearing loss, after accounting for variance associated with age. This effect on hippocampal volume was evident in our sample from age 52 years onwards; when adjusted for hearing loss, the decline began at age 56 years. For the presence of tinnitus, ventral posterior cingulate gyrus showed main effects with respect to cortical volume and surface area while medial occipito-temporal gyrus and operculum of the inferior frontal gyrus showed significant main effects only with surface area. Post-hoc analysis revealed that posterior cingulate gyrus showed significantly higher volume and larger surface area in individuals with tinnitus compared to those without tinnitus. Similarly medial occipito-temporal gyrus surface area was increased whereas surface area of the inferior frontal opercular gyrus was reduced in those with tinnitus when compared to those without tinnitus. Notably, while past studies have reported that the presence of tinnitus appeared to moderate some of these effects in certain participant groups, our results suggest a more complex relationship between sensory degradation, chronic tinnitus, and brain structure in individuals across the adult lifespan. HighlightsO_LIHearing loss and tinnitus can exacerbate regional brain atrophy in the adult lifespan. C_LIO_LIHigh-frequency hearing loss affects auditory cortex gray matter volume to a larger degree in older age. C_LIO_LIHearing loss may accelerate decline in hippocampal volume by about 4 years. C_LIO_LIChronic subjective tinnitus is associated with a larger volume of cingulate cortex, increased surface area in cingulate cortex and the lingual gyrus, and decreased surface area of frontal operculum compared to controls. C_LIO_LITinnitus-related effects on regional brain atrophy are not modified by the degree of hearing deficits. C_LI

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A high-density diffuse optical tomography dataset of naturalistic viewing

Traditional laboratory tasks offer tight experimental control but lack the richness of our everyday human experience. As a result, many cognitive neuroscientists have been motivated to adopt experimental paradigms that are more natural, such as stories and movies. Here we describe data collected from 58 healthy adult participants (aged 18-76 years) who viewed 10 minutes of a movie (The Good, the Bad, and the Ugly, 1966). Most (36) participants viewed the clip more than once, resulting in 106 sessions of data. Cortical responses were mapped using high-density diffuse optical tomography (first-through fourth nearest neighbor separations of 1.3, 3.0, 3.9, and 4.7 cm), covering large portions of superficial occipital, temporal, parietal, and frontal lobes. Consistency of measured activity across subjects was quantified using intersubject correlation analysis. Data are provided in both channel format (SNIRF) and projected to standard space (NIfTI) using an atlas-based light model. These data are suitable for methods exploration as well as investigating a wide variety of cognitive phenomena.

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Real-time feedback reduces participant motion during task-based fMRI

The potential negative impact of head movement during fMRI has long been appreciated. Although a variety of prospective and retrospective approaches have been developed to help mitigate these effects, reducing head movement in the first place remains the most appealing strategy for optimizing data quality. Real-time interventions, in which participants are provided feedback regarding their scan-to-scan motion, have recently shown promise in reducing motion during resting state fMRI. However, whether feedback might similarly reduce motion during task-based fMRI is an open question. In particular, it is unclear whether participants can effectively monitor motion feedback while attending to task-related demands. Here we assessed whether a combination of real-time and between-run feedback could reduce head motion during task-based fMRI. During an auditory word repetition task, 78 adult participants (aged 19-81) were pseudorandomly assigned to receive feedback or not. Feedback was provided FIRMM software that used real-time calculation of realignment parameters to estimate participant motion. We quantified movement using framewise displacement (FD). We found that motion feedback resulted in a statistically significant reduction in participant head motion, with a small-to-moderate effect size (reducing average FD from 0.347 to 0.282). Reductions were most apparent in high-motion events. We conclude that under some circumstances real-time feedback may reduce head motion during task-based fMRI, although its effectiveness may depend on the specific participant population and task demands of a given study.

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Dorsolateral prefrontal cortex supports speech perception in listeners with cochlear implants

Cochlear implants are neuroprosthetic devices that can restore hearing in people with severe to profound hearing loss by electrically stimulating the auditory nerve. Because of physical limitations on the precision of this stimulation, the acoustic information delivered by a cochlear implant does not convey the same level of acoustic detail as that conveyed by normal hearing. As a result, speech understanding in listeners with cochlear implants is typically poorer and more effortful than in listeners with normal hearing. The brain networks supporting speech understanding in listeners with cochlear implants are not well understood, partly due to difficulties obtaining functional neuroimaging data in this population. In the current study, we assessed the brain regions supporting spoken word understanding in adult listeners with right unilateral cochlear implants (n=20) and matched controls (n=18) using high-density diffuse optical tomography (HD-DOT), a quiet and non-invasive imaging modality with spatial resolution comparable to that of functional MRI. We found that while listening to spoken words in quiet, listeners with cochlear implants showed greater activity in left prefrontal cortex than listeners with normal hearing, specifically in a region engaged in a separate spatial working memory task. These results suggest that listeners with cochlear implants require greater cognitive processing during speech understanding than listeners with normal hearing, supported by compensatory recruitment of left prefrontal cortex.

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A multi-dataset evaluation of frame censoring for task-based fMRI

Subject motion during fMRI can affect our ability to accurately measure signals of interest. In recent years, frame censoring--that is, statistically excluding motion-contaminated data within the general linear model using nuisance regressors--has appeared in several task-based fMRI studies as a mitigation strategy. However, there have been few systematic investigations quantifying its efficacy. In the present study, we compared the performance of frame censoring to several other common motion correction approaches for task-based fMRI using open data and reproducible workflows. We analyzed eight publicly-available datasets representing eleven distinct tasks in child, adolescent, and adult participants. Performance was quantified using maximum t-values in group analyses, and ROI-based mean activation and split-half reliability in single subjects. We compared frame censoring across several thresholds to the use of 6 and 24 canonical motion regressors, wavelet despiking, robust weighted least squares, and untrained ICA-based denoising, for a total of 240 separate analyses. Thresholds used to identify censored frames were based on both motion estimates (FD) and image intensity changes (DVARS). Relative to standard motion regressors, we found consistent improvements for modest amounts of frame censoring (e.g., 1-2% data loss), although these gains were frequently comparable to what could be achieved using other techniques. Importantly, no single approach consistently outperformed the others across all datasets and tasks. These findings suggest that the choice of a motion mitigation strategy depends on both the dataset and the outcome metric of interest.

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Increased connectivity among sensory and motor regions during visual and audiovisual speech perception

In everyday conversation, we usually process the talkers face as well as the sound of their voice. Access to visual speech information is particularly useful when the auditory signal is degraded. Here we used fMRI to monitor brain activity while adult humans (n = 60) were presented with visual-only, auditory-only, and audiovisual words. The audiovisual words were presented in quiet and several signal-to-noise ratios. As expected, audiovisual speech perception recruited both auditory and visual cortex, with some evidence for increased recruitment of premotor cortex in some conditions (including in substantial background noise). We then investigated neural connectivity using psychophysiological interaction (PPI) analysis with seed regions in both primary auditory cortex and primary visual cortex. Connectivity between auditory and visual cortices was stronger in audiovisual conditions than in unimodal conditions, including a wide network of regions in posterior temporal cortex and prefrontal cortex. In addition to whole-brain analyses, we also conducted a region-of-interest analysis on the left posterior superior temporal sulcus (pSTS), implicated in many previous studies of audiovisual speech perception. We found evidence for both activity and effective connectivity in pSTS for visual-only and audiovisual speech, although these were not significant in whole-brain analyses. Taken together, our results suggest a prominent role for cross-region synchronization in understanding both visual-only and audiovisual speech that complements activity in "integrative" brain regions like pSTS.

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Age-related differences in auditory cortex activity during spoken word recognition

Understanding spoken words requires the rapid matching of a complex acoustic stimulus with stored lexical representations. The degree to which the brain networks supporting spoken word recognition are affected by adult aging remains poorly understood. In the current study we used fMRI to measure the brain responses to spoken words in two conditions: an attentive listening condition, in which no response was required, and a repetition task. Listeners were 29 young adults (aged 19-30 years) and 32 older adults (aged 65-81 years) without self-reported hearing difficulty. We found largely similar patterns of activity during word perception for both young and older adults, centered on bilateral superior temporal gyrus. As expected, the repetition condition resulted in significantly more activity in areas related to motor planning and execution (including premotor cortex and supplemental motor area) compared to the attentive listening condition. Importantly, however, older adults showed significantly less activity in probabilistically-defined auditory cortex than young adults when listening to individual words in both the attentive listening and repetition tasks. Age differences in auditory cortex activity were seen selectively for words (no age differences were present for 1-channel vocoded speech, used as a control condition), and could not be easily explained by accuracy on the task, movement in the scanner, or hearing sensitivity (available on a subset of participants). These findings indicate largely similar patterns of brain activity for young and older adults when listening to words in quiet, but suggest less recruitment of auditory cortex by the older adults.

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Neural coding of fine-grained object knowledge in perirhinal cortex

SummaryOver 40 years of research has examined the role of the ventral visual stream in transforming retinal inputs into high-level representations of object identity [1-6]. However, there remains an ongoing debate over the role of the ventral stream in coding abstract semantic content, which relies on stored knowledge, versus perceptual content that relies only on retinal inputs [7-12]. A major difficulty in adjudicating between these mechanisms is that the semantic similarity of objects is often highly confounded with their perceptual similarity (e.g., animate things are more perceptually similar to other animate things than to inanimate things). To address this problem, we developed a paradigm that exploits the statistical regularities of object colors while perfectly controlling for perceptual shape information, allowing us to dissociate lower-level perceptual features (i.e., color perception) from higher-level semantic knowledge (i.e., color meaning). Using multivoxel-pattern analyses of fMRI data, we observed a striking double dissociation between the processing of color information at a perceptual and at a semantic level along the posterior to anterior axis of the ventral visual pathway. Specifically, we found that the visual association region V4 assigned similar representations to objects with similar colors, regardless of object category. In contrast, perirhinal cortex, at the apex of the ventral visual stream, assigned similar representations to semantically similar objects, even when this was in opposition to their perceptual similarity. These findings suggest that perirhinal cortex untangles the representational space of lower-level perceptual features and organizes visual objects according to their semantic interpretations.

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