The nature and treatment of stuttering as revealed by fMRI A within- and between-group comparison

This article reviews some of our recent functional magnetic resonance imaging (fMRI) studies of stuttering. Using event-related fMRI experiments, we investigated brain activation during speech production. Results of three studies comparing persons who stutter (PWS) and persons who do not stutter (PWNS) are outlined. Their findings point to a region in the right frontal operculum (RFO) that was consistently implicated in stuttering. During overt reading and before fluency shaping therapy, PWS showed higher and more distributed neuronal activation than PWNS. Immediately after therapy differential activations were even more distributed and left sided. They extended to frontal, temporal, and parietal regions, anterior cingulate, insula, and putamen. These over-activations were slightly reduced and again more right sided two years after therapy. Left frontal deactivations remained stable over two years of observation, and therefore possibly indicate a dysfunction. After therapy, we noted higher activations in persons who stutter moderately than in those who stutter severely. These activations might reflect patterns of compensation. We discuss why these findings suggest that fluency-inducing techniques might synchronize a disturbed signal transmission between auditory, speech motor planning, and motor areas.

Educational objectives: The reader will learn about and be able to: (1) identify regions of brain activations and deactivations specific for PWS; (2) describe brain activation changes induced by fluency shaping therapy; and (3) discuss the correlation between stuttering severity and brain activation.     

The functional anatomy of inspection time: a pilot fMRI study

Seven healthy subjects underwent functional magnetic resonance imaging (fMRI) of the brain while performing an inspection time task. Employing a block-type design, the task had three difficulty levels: a control condition, an easy (200 ms stimulus duration), and a more difficult (40 ms) discrimination. Based on group results, there were widespread significant areas of difference in brain activation and deactivation when pairwise comparisons were conducted among the three task conditions. When the difficult condition was compared with the easy condition, there was relative activation in areas of the following brain regions: cingulate gyrus and some frontal and parietal lobe areas. Areas within the following regions showed relative deactivation (greater blood oxygenation level-dependent, BOLD, signal in the easy condition): frontal, temporal, and parietal lobe. There were overlaps between these areas and those found to be active while performing higher cognitive tasks in other functional brain imaging studies. These pilot data encourage future studies of the functional anatomy of inspection time and its relevance to psychometric intelligence.     

Prosodic processing by children: an fMRI study

Prosodic information in the speech signal carries information about linguistic structure as well as emotional content. Although children are known to use prosodic information from infancy onward to assist linguistic decoding, the brain correlates of this skill in childhood have not yet been the subject of study. Brain activation associated with processing of linguistic prosody was examined in a study of 284 normally developing children between the ages of 5 and 18 years. Children listened to low-pass filtered sentences and were asked to detect those that matched a target sentence. fMRI scanning revealed multiple regions of activation that predicted behavioral performance, independent of age-related changes in activation. Likewise, age-related changes in task activation were found that were independent of differences in task accuracy. The overall pattern of activation is interpreted in light of task demands and factors that may underlie age-related changes in task performance.     

Functional brain activation differences in stuttering identified with a rapid fMRI sequence

The purpose of this study was to investigate whether brain activity related to the presence of stuttering can be identified with rapid functional MRI (fMRI) sequences that involved overt and covert speech processing tasks. The long-term goal is to develop sensitive fMRI approaches with developmentally appropriate tasks to identify deviant speech motor and auditory brain activity in children who stutter closer to the age at which recovery from stuttering is documented. Rapid sequences may be preferred for individuals or populations who do not tolerate long scanning sessions. In this report, we document the application of a picture naming and phoneme monitoring task in 3 min fMRI sequences with adults who stutter (AWS). If relevant brain differences are found in AWS with these approaches that conform to previous reports, then these approaches can be extended to younger populations. Pairwise contrasts of brain BOLD activity between AWS and normally fluent adults indicated the AWS showed higher BOLD activity in the right inferior frontal gyrus (IFG), right temporal lobe and sensorimotor cortices during picture naming and higher activity in the right IFG during phoneme monitoring. The right lateralized pattern of BOLD activity together with higher activity in sensorimotor cortices is consistent with previous reports, which indicates rapid fMRI sequences can be considered for investigating stuttering in younger participants.Educational objectives: The reader will learn about and be able to describe the: (1) use of functional MRI to study persistent developmental stuttering; (2) differences in brain activation between persons who stutter and normally fluent speakers; and (3) potential benefit of time efficient fMRI sequences combined with a range of speech processing tasks for investigating stuttering in younger populations.     

Neural correlates of temporal auditory processing in developmental dyslexia during German vowel length discrimination: an fMRI study

This fMRI study investigated phonological vs. auditory temporal processing in developmental dyslexia by means of a German vowel length discrimination paradigm (Groth, Lachmann, Riecker, Muthmann, & Steinbrink, 2011). Behavioral and fMRI data were collected from dyslexics and controls while performing same-different judgments of vowel duration in two experimental conditions. In the temporal, but not in the phonological condition, hemodynamic brain activation was observed bilaterally within the anterior insular cortices in both groups and within the left inferior frontal gyrus (IFG) in controls, indicating that the left IFG and the anterior insular cortices are part of a neural network involved in temporal auditory processing. Group subtraction analyses did not demonstrate significant effects. However, in a subgroup analysis, participants performing low in the temporal condition (all dyslexic) showed decreased activation of the insular cortices and the left IFG, suggesting that this processing network might form the neural basis of temporal auditory processing deficits in dyslexia.     

Child and mother variables in the development of stuttering among high-risk children: A longitudinal study

In this prospective study, 26 of the 93 preschool children with a parental history of stuttering who began to stutter were compared at preonset and 1 year later with those of a matched group of 26 children who continued to be seen as nonstutterers. These two groups of at-risk children were compared in terms of the development of their articulatory and language skills and in terms of the communicative style and speaking behaviors of their mothers. At preonset, the children who started to stutter demonstrated a faster articulatory rate than those who remained fluent. One year later, however, this difference was no longer statistically significant. The two groups of children did not differ in their linguistic skills at either of these time periods. Moreover, the communicative style and speaking behaviors of the mothers of the children who later began to stutter did not differ from that of the mothers of children who did not either prior to or after the onset of stuttering. This suggests that these variables did not contribute to the onset of stuttering or to its course.     

Towards a functional neural systems model of developmental stuttering

This paper overviews recent developments in an ongoing program of brain imaging research on developmental stuttering that is being conducted at the University of Texas Health Science Center, San Antonio. This program has primarily used H₂¹⁵O PET imaging of different speaking tasks by right-handed adult male and female persistent stutterers, recovered stutterers and controls in order to isolate the neural regions that are functionally associated with stuttered speech. The principal findings have emerged from studies using condition contrasts and performance correlation techniques. The emerging findings from these studies are reviewed and referenced to a neural model of normal speech production recently proposed by Jürgens [Neurosci. Biobehav. Rev. 26 (2002) 235]. This paper will report (1) the reconfiguration of previous findings within the Jürgens Model; (2) preliminary findings of an investigation with late recovered stutterers; (3) an investigation of neural activations during a treatment procedure designed to produce a sustained improvement in fluency; and (4) an across-studies comparison that seeks to isolate neural regions within the Jürgens Model that are consistently associated with stuttering. Two regions appear to meet this criterion: right anterior insula (activated) and anterior middle and superior temporal gyri (deactivated) mainly in right hemisphere. The implications of these findings and the direction of future imaging investigations are discussed.

Educational objectives: The reader will learn about (1) recent uses of H₂¹⁵O PET imaging in stuttering research; (2) the use of a new neurological model of speech production in imaging research on stuttering; and (3) initial findings from PET imaging investigations of treated and recovered stutterers.     

A clinician survey of speech and non-speech characteristics of neurogenic stuttering

This study presents survey data on 58 Dutch-speaking patients with neurogenic stuttering following various neurological injuries. Stroke was the most prevalent cause of stuttering in our patients, followed by traumatic brain injury, neurodegenerative diseases, and other causes. Speech and non-speech characteristics were analyzed separately for these four etiology groups. Results suggested possible group differences, including site of lesion and influence of speech conditions on stuttering. Other characteristics, such as within-word localization of disfluencies and presence of secondary behaviors were comparable across the etiology groups. The implications of our results for the diagnosis of neurogenic stuttering will be discussed.

Educational objectives: After reading this article, the reader will be able to: (1) provide a concise overview of the main literature on neurogenic stuttering; (2) discuss the speech and non-speech characteristics of neurogenic stuttering; (3) provide an overview of current clinical practices for intervention with neurogenic stuttering patients and their perceived outcome.     

Auditory abilities of speakers who persisted, or recovered, from stuttering

OBJECTIVE: The purpose of this study was to see whether participants who persist in their stutter have poorer sensitivity in a backward masking task compared to those participants who recover from their stutter. DESIGN: The auditory sensitivity of 30 children who stutter was tested on absolute threshold, simultaneous masking, backward masking with a broadband and with a notched noise masker. The participants had been seen and diagnosed as stuttering at least 1 year before their 12th birthday. The participants were assessed again at age 12 plus to establish whether their stutter had persisted or recovered. Persistence or recovery was based on participant's, parent's and researcher's assessment and Riley's [Riley, G. D. (1994). Stuttering severity instrument for children and adults (3rd ed.). Austin, TX: Pro-Ed.] Stuttering Severity Instrument-3. Based on this assessment, 12 speakers had persisted and 18 had recovered from stuttering. RESULTS: Thresholds differed significantly between persistent and recovered groups for the broadband backward-masked stimulus (thresholds being higher for the persistent group). CONCLUSIONS: Backward masking performance at teenage is one factor that distinguishes speakers who persist in their stutter from those who recover. Education objectives: Readers of this article should: (1) explain why auditory factors have been implicated in stuttering; (2) summarise the work that has examined whether peripheral, and/or central, hearing are problems in stuttering; (3) explain how the hearing ability of persistent and recovered stutterers may differ; (4) discuss how hearing disorders have been implicated in other language disorders.     

Developmental shifts in fMRI activations during visuospatial relational reasoning

To investigate maturational plasticity of fluid cognition systems, functional brain imaging was undertaken in healthy 8-19 year old participants while completing visuospatial relational reasoning problems similar to Raven's matrices and current elementary grade math textbooks. Analyses revealed that visuospatial relational reasoning across this developmental age range recruited activations in the superior parietal cortices most prominently, the dorsolateral prefrontal, occipital-temporal, and premotor/supplementary cortices, the basal ganglia, and insula. There were comparable activity volumes in left and right hemispheres for nearly all of these regions. Regression analyses indicated increasing activity predominantly in the superior parietal lobes with developmental age. In contrast, multiple anterior neural systems showed significantly less activity with age, including dorsolateral and ventrolateral prefrontal, paracentral, and insula cortices bilaterally, basal ganglia, and particularly large clusters in the midline anterior cingulate/medial frontal cortex, left middle cingulate/supplementary motor cortex, left insula-putamen, and left caudate. Findings suggest that neuromaturational changes associated with visuospatial relational reasoning shift from a more widespread fronto-cingulate-striatal pattern in childhood to predominant parieto-frontal activation pattern in late adolescence.     

Dissociable patterns of brain activity during comprehension of rapid and syntactically complex speech: evidence from fMRI

Sentence comprehension is a complex task that involves both language-specific processing components and general cognitive resources. Comprehension can be made more difficult by increasing the syntactic complexity or the presentation rate of a sentence, but it is unclear whether the same neural mechanism underlies both of these effects. In the current study, we used event-related functional magnetic resonance imaging (fMRI) to monitor neural activity while participants heard sentences containing a subject-relative or object-relative center-embedded clause presented at three different speech rates. Syntactically complex object-relative sentences activated left inferior frontal cortex across presentation rates, whereas sentences presented at a rapid rate recruited frontal brain regions such as anterior cingulate and premotor cortex, regardless of syntactic complexity. These results suggest that dissociable components of a large-scale neural network support the processing of syntactic complexity and speech presented at a rapid rate during auditory sentence processing.     

Lying about facial recognition: an fMRI study

Novel deception detection techniques have been in creation for centuries. Functional magnetic resonance imaging (fMRI) is a neuroscience technology that non-invasively measures brain activity associated with behavior and cognition. A number of investigators have explored the utilization and efficiency of fMRI in deception detection. In this study, 18 subjects were instructed during an fMRI "line-up" task to either conceal (lie) or reveal (truth) the identities of individuals seen in study sets in order to determine the neural correlates of intentionally misidentifying previously known faces (lying about recognition). A repeated measures ANOVA (lie vs. truth and familiar vs. unfamiliar) and two paired t-tests (familiar vs. unfamiliar and familiar lie vs. familiar truth) revealed areas of activation associated with deception in the right MGF, red nucleus, IFG, SMG, SFG (with ACC), DLPFC, and bilateral precuneus. The areas activated in the present study may be involved in the suppression of truth, working and visuospatial memories, and imagery when providing misleading (deceptive) responses to facial identification prompts in the form of a "line-up".     

Evaluation of the efficacy of a stutter modification program with particular reference to two new measures of secondary behaviors and control of stuttering

This study aimed to assess the changes in speech behaviors and attitudes of a group of stutterers who attended an intensive stutter modification program, using measures specifically designed to reflect the aims of the program. These included a measure of “clean” stuttering to quantify overt secondary behaviors and a quantitative measure of speech control to assess changes in control over stuttering moments using the taught handling techniques. High interjudge and intrajudge agreement was obtained on the two new speech measures. In addition, the program’s own Attitude Scale was used to assess changes in attitudes toward communication. The five subjects were assessed immediately after and 2 years after the program. Each subject was analyzed as a single case study, and there was great individual variation in response to therapy. The general trend was a decline in the maintenance of speech behaviors, with good maintenance of attitude gains 2 years postworkshop. The poorest maintenance was linked to lack of attendance at refresher therapy and initial severity of stuttering. The two new measures used to evaluate change in clean stuttering and control may be useful tools in the assessment protocol of other Stutter Modification programs.     

Changes in brain activation induced by the training of hypothesis generation skills: an fMRI study

The aim of the present study is to investigate the learning-related changes in brain activation induced by the training of hypothesis generation skills regarding biological phenomena. Eighteen undergraduate participants were scanned twice with functional magnetic resonance imaging (fMRI) before and after training over a period of 2 months. The experimental group underwent eight biological hypothesis generation training programs, but the control group was not given any during the 2-month period. The results showed that the left frontal gyri, the cingulate gyrus, and the cuneus were activated during hypothesis generation. In addition, the brain activation of the trained group increased in the left inferior and the superior frontal gyri, which are related to working memory load and higher-order inferential processes. However, the activation after training decreased in the occipito-parietal route, which is associated with the perception and the analysis processes of visual information. Furthermore, the results have suggested that the dorsolateral prefrontal cortex (DLPFC) region is the critical area in the training of hypothesis generation skills.     

Persistence and remission of incipient stuttering among high-risk children

This investigation concerns the persistence of stuttering and recovery from it among high-risk children. At the end of the second year of a 6-year prospective study, 26 of 93 preschool children with a parental history of stuttering were classified as stutterers. Four years later, seven of these children were classified as persistent stutterers, and 16 children were classified as recovered stutterers. The articulatory and linguistic skills of these two groups of children and the communicative and speaking behaviors of their mothers, were measured before and after the onset of stuttering. The analysis of these measures revealed that the articulatory skills of the children and the communicative style and language complexity of the mothers differentiated the incipient stutters whose stuttering subsequently became chronic from those who recovered.     

Public awareness and knowledge of stuttering in Rio de Janeiro

This study reports the results of an investigation of public awareness and knowledge of stuttering in Rio de Janeiro, Brazil. A total number of 606 street recruited respondents answered questions on various aspects of stuttering, including prevalence, onset, gender distribution, occurrence in different cultures, cause, treatment, intelligence, and hereditariness. The questionnaire used was a Portuguese version of the one by [Van Borsel, J., Verniers, I. & Bouvry, S. (1999). Public awareness of stuttering. Folia Phoniatrica et Logopaedica, 51, 124–132]. Although, stuttering is a disorder which is known to a majority of the participants, knowledge appears to be limited for certain aspects. Knowledge also differs among subgroups of participants according to gender, age and educational level. Comparison of the results of the current study with similar studies conducted in Belgium and in Shanghai, China shows several similarities but also some differences.

Educational objectives: The reader will be able to: (1) discuss public awareness and knowledge of stuttering in Rio de Janeiro, Brazil; (2) discuss the differences in knowledge according to gender, age and educational level and; (3) discuss similarities and differences with comparable studies run in Belgium and Shanghai, China.     

Attention and semantic processing during speech: an fMRI study

This fMRI study was conducted to investigate whether language semantics is processed even when attention is not explicitly directed to word meanings. In the “unattended” condition, the subjects performed a visual detection task while hearing semantically related and unrelated word pairs. In the “phoneme” condition, the subjects made phoneme judgements between prime and target words, and in the “word” condition, they indicated whether the words in each word pair were semantically related or unrelated. In the word condition, stronger activity was obtained for unrelated than related words in the superior temporal gyrus/sulcus (STG/STS), lingual/fusiform gyri and cuneus, whereas in the phoneme condition no such effect was observed. However, during the unattended condition, stronger activity was found in the right STG. Our results suggest that both semantic judgement of word pairs and their passive hearing activate the same neural networks but this activation is more restricted in the passive hearing.     

fMRI of parents of children with Asperger Syndrome: a pilot study

BACKGROUND: People with autism or Asperger Syndrome (AS) show altered patterns of brain activity during visual search and emotion recognition tasks. Autism and AS are genetic conditions and parents may show the 'broader autism phenotype.' AIMS: (1) To test if parents of children with AS show atypical brain activity during a visual search and an empathy task; (2) to test for sex differences during these tasks at the neural level; (3) to test if parents of children with autism are hyper-masculinized, as might be predicted by the 'extreme male brain' theory. METHOD: We used fMRI during a visual search task (the Embedded Figures Test (EFT)) and an emotion recognition test (the 'Reading the Mind in the Eyes' (or Eyes) test). SAMPLE: Twelve parents of children with AS, vs. 12 sex-matched controls. DESIGN: Factorial analysis was used to map main effects of sex, group (parents vs. controls), and sexxgroup interaction on brain function. An ordinal ANOVA also tested for regions of brain activity where females>males>fathers=mothers, to test for parental hyper-masculinization. RESULTS ON EFT TASK: Female controls showed more activity in extrastriate cortex than male controls, and both mothers and fathers showed even less activity in this area than sex-matched controls. There were no differences in group activation between mothers and fathers of children with AS. The ordinal ANOVA identified two specific regions in visual cortex (right and left, respectively) that showed the pattern Females>Males>Fathers=Mothers, both in BA 19. RESULTS ON EYES TASK: Male controls showed more activity in the left inferior frontal gyrus than female controls, and both mothers and fathers showed even more activity in this area compared to sex-matched controls. Female controls showed greater bilateral inferior frontal activation than males. This was not seen when comparing mothers to males, or mothers to fathers. The ordinal ANOVA identified two specific regions that showed the pattern Females>Males>Mothers=Fathers: left medial temporal gyrus (BA 21) and left dorsolateral prefrontal cortex (BA 44). CONCLUSIONS: Parents of children with AS show atypical brain function during both visual search and emotion recognition, in the direction of hyper-masculinization of the brain. Because of the small sample size, and lack of age-matching between parents and controls, such results constitute a pilot study that needs replicating with larger samples.