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RAIND Project:Neural Mechanisms of Developmental Stuttering: Translation of an Animal Model of Rhythm Processing to Assessment and Intervention

J. Devin McAuleyDepartment of Psychology and Neuroscience ProgramMichigan State University

Collaborators: Soo-Eun Chang, Laura Dilley, and Juli Wade

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2Time and Rhythm in the Worldhttp://www.youtube.com/watch?v=DcfW_hlYZ5k

McAuley et al., 2006, JEP: GENDevelopmental Changes in Preferred Tempo 3

Implications of Rhythm and Entrainment

Dynamic Allocation of Attention in TimeLanguage Development4

Rhythm and Language Development

Rhythm skills important for normal language development, including:Phonological awareness (Moritz et al., 2013)Morpho-syntactic competence (Gordon et al., 2014, 2015)Rhythm/temporal deficits implicated in:Developmental dyslexia (Goswami, 2011)SLI (Corriveau et al., 2007)Developmental stuttering (Wieland et al., 2015)5

The importance of rhythmic ability in the development of language skills, in speech and in print, is increasingly well-documented. The broad range of neurodevelopmental disorders that implicate rhythm and/or temporal processingas a core deficit is indeed quite striking. These include developmental stuttering, developmentaldyslexia, and specific language impairment (SLI), among others. This symposium bringstogether four scholars working at the intersection of musical rhythm and language to addresstwo related themes. First, although rhythm appears to play a central role in normal languagedevelopment, the specific nature of rhythm and/or temporal processing deficits in differentlanguage disorders is not yet clear. Second, given that rhythm processing has been identifiedas a core deficit in language disorders, to what extent can rhythm-based therapies serve as aneffective intervention?

Toward these ends, Dr. Devin McAuley (Michigan State University) will present research from theirgroup revealing both rhythm discrimination impairments in developmental stuttering, andreduced functional connectivity in the basal ganglia-thalamic-cortical network previouslyimplicated in rhythm perception. Dr. Ioulia Kovelman (University of Michigan) will presenta developmental neuroimaging studying suggesting that at least by the age childrenreach elementary school, it is the efficiency with which left temporal regions process slowtemporal information that is important for gains in language and reading proficiency. Dr. JenniferThomson (University of Sheffield) will discuss the relationship between rhythm and literacyskills and consider the effectiveness of a rhythm-based intervention on improving phonologicalawareness in developmental dyslexia. Finally, Dr. Reyna Gordon (Vanderbilt University) willpresent recent research showing a relationship between rhythm discrimination and grammarskills and will discuss the implications for developing rhythm-based interventions in SLI.5

Developmental StutteringChronic stuttering affects a significant portion of the population (~ 3 million individuals in the US)

Children who develop chronic stuttering face lifelong struggles that can impact academic achievement and lead to negative psychosocial consequences.

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Developmental StutteringStuttering is characterized by frequent occurrences of repetitions and/or prolongations of sounds, syllables, or words, and/or frequent hesitations or pauses.

Disfluencies are typically marked as a disorder if they disrupt the rhythmic flow of speech (World-Health-Organization, 2010). 7

Developmental StutteringStuttering onset is typically between 3 and 5 years, when children are first putting words together into sentences. Up to 70-80% experience full recovery (Andrews et al., 1983; Yairi & Ambrose, 1999). Neural mechanisms of developmental stuttering, including reasons that some children recover, are poorly understood.

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Stuttering is notoriously difficult to treat. Behavioral interventions can reduce symptoms but relapse is common and no cure exists. 8

Developmental StutteringStuttering can be markedly alleviated when

Synchronizing speech with a metronome (Wingate, 2002; Wohl, 1968)Speaking in unison with another (Adams & Ramig, 1980; Ingham & Carroll, 1977)Singing (Glover, Kalinowski, Rastatter, & Stuart, 1996) 9

Rhythm Hypothesis

Metronome, choral speech, and singing, may induce fluencyin people who stutter, due to the fact that these methods provides an external pacing signal (i.e., a rhythm).

This suggests that individuals who stutter may have a deficit in one aspect of rhythm perception internal beat generation.

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Grahn, Henry & McAuley (2011)

12Grahn & McAuley (2009)

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Resting state fMRI data showing functional connectivity analyses for 46 children between 3-9 years of age (Chang & Zhu, 2013). Functional connectivity between L SMA and L Putamen was weaker in children who stutter compared to controls. Chang & Zhu (2013)

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Rhythm Perception in Children who Stutter(Wieland et al., Brain & Language, 2015)

The task was presented in the context of a computer game, where Randy Drummer would play the standard rhythm two times and then either the same rhythm would be played back to Randy by his twin brother Sandy Same or a different rhythm would be played back by his friend Doggy Different. Children indicated whether the third rhythm was being played by Sandy Same (who played the same rhythm) or Doggy Different (who played a different rhythm) by pressing the a button on the keyboard.14

MethodsParticipants17 typically developing children (9 F, 8 M)17 children who stutter (9 F, 8 M)Ages, 6 11 yearsMonolingual, native speakers of EnglishNormal hearingAll given speech, language and cognitive battery15

MethodsProcedureSame-Different Rhythm Discrimination28 trials (14 simple, 14 complex)Tempo varies from trial to trial

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Results17

CWNSCWSCWS - CWNSModulatory effects of collapsed d on functional connectivity

Seed Region: Left PutamenRegions whose functional connectivity with the left putamen positively modulated by collapsed dRegions whose functional connectivity with the left putamen negatively modulated by collapsed d

Songbirds as an Animal Model of Rhythm(Lampen et al., PLoS One, 2014)19

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ConclusionsFirst demonstration of a rhythm perception deficit in children who stutter.Same impairment observed in adults who stutterBehavioral differences not attributable to differences in cognitive ability.Relationship between rhythm perception and functional connectivity in rhythm network.Songbird work provides evidence that the zebra finch is a viable model of rhythm processing.

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Current and Future WorkfMRI study of adults in analysis stage; in process of extending fMRI work to children.TMS and tDCS techniques will be used to modulate neural function; the latter has potential for clinically relevant functional improvement.Current zebra finch work is examining developmental trajectory of neural responses to rhythm; this will be combined with lesion studies to probe neural mechanisms of rhythm processing.New NIH R03 grant with Vanderbilt University examining rhythm perception in SLI.

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AcknowledgmentsSoo-Eun Chang, University of Michigan & MSUJuli Wade, MSULiz Wieland, MSULaura Dilley, MSUEllie Kim Fromboluti, MSULauren Amick, MSUTuuli Morrill, GMUKatherine Jones, MSUJennifer Lampen, MSUReyna Gordon, Vanderbilt UniversityKarli Nave, UNLVMolly Henry, Western UniversityJessica Grahn, Western University

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MethodsStimuli7 simple and 7 complex rhythms

5,6, 7 intervals longBase inter-onset-inteval (IOI): 165 205 msAll intervals a multiple of base IOI: 1x, 2x, 3x, 4x24

MeasureControlsStuttering ChildrenAge (years)8.8 (1.5)8.7 (1.6)Full IQ112.2 (15.4)106.2 (13.6)Performance IQ111.7 (16.2)107.9 (11.5)Verbal IQ110.8 (14.1)103.3 (14.5)PPVT-4* 110.2 (8.9)101.4 (10.6)% Disfluencies**0.8 (0.6)3.6 (2.8)

25*p < 0.05; **p < 0.01

ZENK SummaryIncreased neural activity for arhythmic stimuli in NCM and CMM parallels increased activity in the human auditory cortex following exposure to unexpected, or perturbed, auditory stimuli. NCM and CMM may be detecting errors in arrhythmic song when comparing it to a stored template of how conspecific song is expected to sound. CMM may also be important for females in evaluating songs of potential mates.

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