Evidence of the role of the cerebellum in cognitive theory of mind using voxel-based lesion mapping.

Theory of Mind (ToM) is a social-cognitive skill that allows the understanding of the intentions, beliefs, and desires of others. There is a distinction between affective and cognitive ToM, with evidence showing that these processes rely on partially distinct neural networks. The role of the cerebellum in social cognition has only been rarely explored. In this study, we tested whether the cerebellum is necessary for cognitive and affective ToM performance. We investigated adults with traumatic brain injury (n = 193) and healthy controls (n = 52) using voxel-based lesion-symptom mapping (VLSM) and by measuring the impact on functional connectivity. First, we observed that damage to the cerebellum affected pure Cognitive ToM processing. Further, we found a lateralization effect for the role of the cerebellum in cognitive ToM with participants with left cerebellar injury performing worse than those with right cerebellar injury. Both VLSM and standard statistical analysis provided evidence that left cerebellar Crus I and lobule VI contributed to ToM processing. Lastly, we found that disconnection of the left thalamic projection and the left fronto-striatal fasciculus was associated with poor cognitive ToM performance. Our study is the first to reveal direct causal neuropsychological evidence for a role of the cerebellum in some but not all types of ToM, processing. It reinforces the idea that social cognition relies on a complex network functionally connected through white matter pathways that include the cerebellum. It supports evidence that the neural networks underpinning the different types of ToM can be differentiated.

The neural basis for mental state attribution: A voxel-based lesion mapping study.

The ability to infer other persons' mental states, "Theory of Mind" (ToM), is a key function of social cognition and is needed when interpreting the intention of others. ToM is associated with a network of functionally related regions, with reportedly key prominent hubs located in the dorsolateral prefrontal cortex (dlPFC) and the temporoparietal junction (TPJ). The involvement of (mainly the right) TPJ in ToM is based primarily on functional imaging studies that provide correlational evidence for brain-behavior associations. In this lesion study, we test whether certain brain areas are necessary for intact ToM performance. We investigated individuals with penetrating traumatic brain injury (n = 170) and healthy matched controls (n = 30) using voxel-based lesion-symptom mapping (VLSM) and by measuring the impact of a given lesion on white matter disconnections. ToM performance was compared between five patient groups based on lesion location: right TPJ, left TPJ, right dlPFC, left dlPFC, and other lesion, as well as healthy controls. The only group to present with lower ToM abilities was the one with lesions in the right dlPFC. Similarly, VLSM analysis revealed a main cluster in the right frontal middle gyrus and a secondary cluster in the left inferior parietal gyrus. Last, we found that disconnection of the left inferior longitudinal fasciculus and right superior longitudinal fasciculus were associated with poor ToM performance. This study highlights the importance of lesion studies in complementing functional neuroimaging findings and supports the assertion that the right dlPFC is a key region mediating mental state attribution.

Distinct neural networks for detecting violations of adjacent versus nonadjacent sequential dependencies: An fMRI study.

The ability to learn and process sequential dependencies is essential for language acquisition and other cognitive domains. Recent studies suggest that the learning of adjacent (e.g., "A-B") versus nonadjacent (e.g., "A-X-B") dependencies have different cognitive demands, but the neural correlates accompanying such processing are currently underspecified. We developed a sequential learning task in which sequences of printed nonsense syllables containing both adjacent and nonadjacent dependencies were presented. After incidentally learning these grammatical sequences, twenty-one healthy adults (age M = 22.1, 12 females) made familiarity judgments about novel grammatical sequences and ungrammatical sequences containing violations of the adjacent or nonadjacent structure while in a 3T MRI scanner. Violations of adjacent dependencies were associated with increased BOLD activation in both posterior (lateral occipital and angular gyrus) as well as frontal regions (e.g., medial frontal gyrus, inferior frontal gyrus). Initial results indicated no regions showing significant BOLD activations for the violations of nonadjacent dependencies. However, when using a less stringent cluster threshold, exploratory analyses revealed that violations of nonadjacent dependencies were associated with increased activation in subcallosal cortex, paracingulate cortex, and anterior cingulate cortex (ACC). Finally, when directly comparing the adjacent condition to the nonadjacent condition, we found significantly greater levels of activation for the right superior lateral occipital cortex (BA 19) for the adjacent relative to nonadjacent condition. In sum, the detection of violations of adjacent and nonadjacent dependencies appear to involve distinct neural networks, with perceptual brain regions mediating the processing of adjacent but not nonadjacent dependencies. These results are consistent with recent proposals that statistical-sequential learning is not a unified construct but depends on the interaction of multiple neurocognitive mechanisms acting together.

A New Insight on the Role of the Cerebellum for Executive Functions and Emotion Processing in Adults.

Objective: We investigated whether the cerebellum plays a critical or supportive role in in executive and emotion processes in adults. Many investigators now espouse the hypothesis that participants with cerebellar lesions experience executive functions and emotions (EE) disorders. But we hypothesized that these disorders would be milder if the damage is relatively limited to the cerebellum compared to damage involving the cerebellum plus additional cortical areas. Methods: We studied veterans with penetrating Traumatic Brain Injury (pTBI) participating in the Vietnam Head Injury Study (VHIS). We selected veterans with a cerebellar lesion (n = 24), a prefrontal cortex lesion (n = 20), along with healthy controls (HC) (n = 55). Tests of executive functions and emotions were analyzed as well as caregiver burden. We performed between-group null hypothesis significance testing, Bayesian hypothesis tests and correlational analyses. Results: Performance of participants with cerebellar lesions which extended to the cerebral cortex was similar to the HC on the Executive Function tests but they were significantly impaired on the Working Memory Index. No differences were found on the emotional processing tasks with one exception-the Facial Expression of Emotion-Test (FEEST). We then examined a sub-group of participants with large cerebellar lesions (>15%) but minimal lesions in the cerebral cortex (<15%). This sub-group of participants performed similarly to the HC on the Working Memory Index and on the FEEST. Conclusions: We suggest that the cerebellar cortex may not be critical for executive functions or processing emotional stimuli in adults as suggested. Instead, we find that the cerebellum has a supportive role characterized by its computing of the motor requirements when EE processing is required.

High-Variability Sentence Recognition in Long-Term Cochlear Implant Users: Associations With Rapid Phonological Coding and Executive Functioning.

OBJECTIVES: The objective of the present study was to determine whether long-term cochlear implant (CI) users would show greater variability in rapid phonological coding skills and greater reliance on slow-effortful compensatory executive functioning (EF) skills than normal-hearing (NH) peers on perceptually challenging high-variability sentence recognition tasks. We tested the following three hypotheses: First, CI users would show lower scores on sentence recognition tests involving high speaker and dialect variability than NH controls, even after adjusting for poorer sentence recognition performance by CI users on a conventional low-variability sentence recognition test. Second, variability in fast-automatic rapid phonological coding skills would be more strongly associated with performance on high-variability sentence recognition tasks for CI users than NH peers. Third, compensatory EF strategies would be more strongly associated with performance on high-variability sentence recognition tasks for CI users than NH peers. DESIGN: Two groups of children, adolescents, and young adults aged 9 to 29 years participated in this cross-sectional study: 49 long-term CI users (≥7 years) and 56 NH controls. All participants were tested on measures of rapid phonological coding (Children's Test of Nonword Repetition), conventional sentence recognition (Harvard Sentence Recognition Test), and two novel high-variability sentence recognition tests that varied the indexical attributes of speech (Perceptually Robust English Sentence Test Open-set test and Perceptually Robust English Sentence Test Open-set test-Foreign Accented English test). Measures of EF included verbal working memory (WM), spatial WM, controlled cognitive fluency, and inhibition concentration. RESULTS: CI users scored lower than NH peers on both tests of high-variability sentence recognition even after conventional sentence recognition skills were statistically controlled. Correlations between rapid phonological coding and high-variability sentence recognition scores were stronger for the CI sample than for the NH sample even after basic sentence perception skills were statistically controlled. Scatterplots revealed different ranges and slopes for the relationship between rapid phonological coding skills and high-variability sentence recognition performance in CI users and NH peers. Although no statistically significant correlations between EF strategies and sentence recognition were found in the CI or NH sample after use of a conservative Bonferroni-type correction, medium to high effect sizes for correlations between verbal WM and sentence recognition in the CI sample suggest that further investigation of this relationship is needed. CONCLUSIONS: These findings provide converging support for neurocognitive models that propose two channels for speech-language processing: a fast-automatic channel that predominates whenever possible and a compensatory slow-effortful processing channel that is activated during perceptually-challenging speech processing tasks that are not fully managed by the fast-automatic channel (ease of language understanding, framework for understanding effortful listening, and auditory neurocognitive model). CI users showed significantly poorer performance on measures of high-variability sentence recognition than NH peers, even after simple sentence recognition was controlled. Nonword repetition scores showed almost no overlap between CI and NH samples, and correlations between nonword repetition scores and high-variability sentence recognition were consistent with greater reliance on engagement of fast-automatic phonological coding for high-variability sentence recognition in the CI sample than in the NH sample. Further investigation of the verbal WM-sentence recognition relationship in CI users is recommended. Assessment of fast-automatic phonological processing and slow-effortful EF skills may provide a better understanding of speech perception outcomes in CI users in the clinical setting.

The Role of Statistical Learning in Understanding and Treating Spoken Language Outcomes in Deaf Children With Cochlear Implants.

Purpose: Statistical learning-the ability to learn patterns in environmental input-is increasingly recognized as a foundational mechanism necessary for the successful acquisition of spoken language. Spoken language is a complex, serially presented signal that contains embedded statistical relations among linguistic units, such as phonemes, morphemes, and words, which represent the phonotactic and syntactic rules of language. In this review article, we first review recent work that demonstrates that, in typical language development, individuals who display better nonlinguistic statistical learning abilities also show better performance on different measures of language. We next review research findings that suggest that children who are deaf and use cochlear implants may have difficulties learning sequential input patterns, possibly due to auditory and/or linguistic deprivation early in development, and that the children who show better sequence learning abilities also display improved spoken language outcomes. Finally, we present recent findings suggesting that it may be possible to improve core statistical learning abilities with specialized training and interventions and that such improvements can potentially impact and facilitate the acquisition and processing of spoken language. Method: We conducted a literature search through various online databases including PsychINFO and PubMed, as well as including relevant review articles gleaned from the reference sections of other review articles used in this review. Search terms included various combinations of the following: sequential learning, sequence learning, statistical learning, sequence processing, procedural learning, procedural memory, implicit learning, language, computerized training, working memory training, statistical learning training, deaf, deafness, hearing impairment, hearing impaired, DHH, hard of hearing, cochlear implant(s), hearing aid(s), and auditory deprivation. To keep this review concise and clear, we limited inclusion to the foundational and most recent (2005-2018) relevant studies that explicitly included research or theoretical perspectives on statistical or sequential learning. We here summarize and synthesize the most recent and relevant literature to understanding and treating language delays in children using cochlear implants through the lens of statistical learning. Conclusions: We suggest that understanding how statistical learning contributes to spoken language development is important for understanding some of the difficulties that children who are deaf and use cochlear implants might face and argue that it may be beneficial to develop novel language interventions that focus specifically on improving core foundational statistical learning skills.

Can we improve structured sequence processing? Exploring the direct and indirect effects of computerized training using a mediational model.

Recent research suggests that language acquisition may rely on domain-general learning abilities, such as structured sequence processing, which is the ability to extract, encode, and represent structured patterns in a temporal sequence. If structured sequence processing supports language, then it may be possible to improve language function by enhancing this foundational learning ability. The goal of the present study was to use a novel computerized training task as a means to better understand the relationship between structured sequence processing and language function. Participants first were assessed on pre-training tasks to provide baseline behavioral measures of structured sequence processing and language abilities. Participants were then quasi-randomly assigned to either a treatment group involving adaptive structured visuospatial sequence training, a treatment group involving adaptive non-structured visuospatial sequence training, or a control group. Following four days of sequence training, all participants were assessed with the same pre-training measures. Overall comparison of the post-training means revealed no group differences. However, in order to examine the potential relations between sequence training, structured sequence processing, and language ability, we used a mediation analysis that showed two competing effects. In the indirect effect, adaptive sequence training with structural regularities had a positive impact on structured sequence processing performance, which in turn had a positive impact on language processing. This finding not only identifies a potential novel intervention to treat language impairments but also may be the first demonstration that structured sequence processing can be improved and that this, in turn, has an impact on language processing. However, in the direct effect, adaptive sequence training with structural regularities had a direct negative impact on language processing. This unexpected finding suggests that adaptive training with structural regularities might potentially interfere with language processing. Taken together, these findings underscore the importance of pursuing designs that promote a better understanding of the mechanisms underlying training-related changes, so that regimens can be developed that help reduce these types of negative effects while simultaneously maximizing the benefits to outcome measures of interest.

REHABILITATING LANGUAGE DISORDERS BY IMPROVING SEQUENTIAL PROCESSING: A REVIEW.

Recent research suggests that language processing (LP) may rely heavily on sequential processing (SP), a cognitive ability that allows people to process the patterns of environmental stimuli that unfold in time, such as spoken language or music. Indeed, spoken language corresponds to a set of linguistic units (e.g., phonemes, syllables, words) that are organized in time in a non-random way, according to phonotactic and syntactic rules. In this review, we discuss recent research highlighting the importance of SP for learning and processing such linguistic regularities and argue that interventions focused on improving SP may provide a potentially effective way to rehabilitate language impairments. The first part of this review presents a series of findings showing that LP is intimately related to SP. We review the literature on populations with normal LP performance suggesting that LP relies upon SP. We then report two recent studies from our lab that demonstrated a direct link between LP and SP: (1) a behavioral study showing that variations on a non-linguistic SP task are significantly associated with LP, and (2) an event-related potential study showing that the neural correlates of SP interact with LP abilities in healthy adults. The second part of this review summarizes the literature suggesting that populations with LP impairments (such as language delays due to hearing loss, dyslexia, specific language impairment, and aphasia) also display SP impairments. Thus, disturbances to SP appear to be a commonality among what appears to be very different types of LP impairments, suggesting that impaired SP causes or exacerbates LP impairment. This leads to the third part of this review, where we first summarize recent findings from brain plasticity showing that: (1) cognitive training can improve cognitive processing, and that (2) increasing cognitive processing performance through training can result in a cognitive "transfer" by also increasing performance on other related cognitive skills. We then present a potentially new method for LP remediation that is based on the idea that some LP impairments might stem directly from SP disturbances and that improving SP processing will, via transfer, result in increased LP performance. This method was applied by our research team to conduct a study aimed at improving SP and LP mechanisms. To our knowledge, the SP training study presented here shows the first evidence that SP performance can be improved and therefore has strong clinical implications as a potentially effective and novel intervention to treat LP impairments.