The Linguistic Cerebellum

The Linguistic Cerebellum provides a comprehensive analysis of this unique part of the brain that has the most number of neurons, each operating in distinct networks to perform diverse functions.

This book outlines how those distinct networks operate in relation to non-motor language skills. Coverage includes cerebellar anatomy and function in relation to speech perception, speech planning, verbal fluency, grammar processing, and reading and writing, along with a discussion of language disorders.

• Discusses the neurobiology of cerebellar language functions, encompassing both normal language function and language disorders
• Includes speech perception, processing, and planning
• Contains cerebellar function in reading and writing
• Explores how language networks give insight to function elsewhere in the brain

• Language: English
• Publisher: Academic Press
• Release date: Sep 7, 2015
• ISBN: 9780128017852

Book preview

The Linguistic Cerebellum

Editors

Peter Mariën

Department of Neurology and Memory Clinic, ZNA Middelheim General Hospital, Antwerp, Belgium

Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

Mario Manto

Unité d’Etude du Mouvement Université Libre de Bruxelles, Brussels, Belgium

Université de Mons, Mons, Belgium

Table of Contents

Cover image

Title page

Copyright

Contributors

Introduction

Chapter 1. The Phonetic Cerebellum: Cerebellar Involvement in Speech Sound Production

Introduction

Cerebellar Contributions to Speech: Neuroanatomical Basis

Clinical Evidence

Conclusion: Models of Cerebellar Function in Speaking

Chapter 2. The Role of the Cerebellum in Speech Perception and Language Comprehension

Introduction

Cerebellar Aspects of Primary Auditory Functions

Speech Timing and Phonology

Higher Order Aspects of Speech Comprehension

Interference and Attention

Working Memory

Inner Speech and the Action Theory of Perception

Cognitive Automation

Chapter 3. The Cerebellum and Verbal Working Memory

Chapter 4. Cerebellum and Verbal Fluency (Phonological and Semantic)

Introduction

Neural Correlate of Verbal Fluency

Verbal Fluency in Cerebellar Pathologies

Clustering and Switching

Mechanism of Cerebellar Involvement in Verbal Fluency

Sequence Detection Theory

Conclusions

Chapter 5. Cerebellum and Grammar Processing

Background

Clinical Data

Neuroanatomical Architecture of the Cerebellum in Grammar Operations

Neurophysiologic Features of the Cerebellum in Grammar Processing

Theoretical Considerations of Underlying Cerebrocerebellar Pathways

Discussion

Chapter 6. Cerebellar-Induced Aphasia and Related Language Disorders

Introduction

Cerebellum and Linguistic Impairments

Cerebellar-Induced Aphasia

Discussion

Conclusion

Chapter 7. Analysis of Speech and Language Impairments in Cerebellar Disorders

Introduction

Voice Recording Material

Voice Recording Session

Analysis Algorithm and Effects

Spinocerebellar Ataxia Diagnosis Using Speech Analysis

Acoustic Findings in Cerebellar Patients

Conclusion

Chapter 8. Cerebellum and Writing

Introduction

Writing

Agraphia

Cerebellum

Discussion

Conclusion

Chapter 9. The Role of the Cerebellum in Developmental Dyslexia

Introduction

Is the Cerebellum Part of the Reading Network?

Does Cerebellar Damage Cause Reading Difficulties?

Neuroimaging Evidence of Differences in Cerebellar Structure and Function in Dyslexia

Behavioral Manifestations of Cerebellar Dysfunction in Dyslexic Readers

The Cerebellum, Internal Models, and Procedural Learning: Impact on Literacy Acquisition and Remediation?

Conclusion

Chapter 10. Conceptualizing Developmental Language Disorders: A Theoretical Framework Including the Role of the Cerebellum in Language-Related Functioning

Introduction

Why Bother to Include the Cerebellum?

The Vertebrate Brain: Neocortex, Basal Ganglia, and Cerebellum

Classification of Developmental Language Disorders

Language Science and Brain Systems

Large-Scale Brain Systems

The Novelty-Routinization Principle: Neurobiologic Consistency and the Vertebrate Brain

The Declarative-Procedural Model of Language

The Role of the Cerebellum in Language Functions

Bottom-Up Development: Early Prediction of Language Outcomes

Linguistic Development and Disorders of Language

Summary and Conclusions

Chapter 11. Posterior Fossa Syndrome (PFS) and Cerebellar Mutism

Introduction

Historical Overview

Clinical Characteristics

Definitions and Abbreviations

The Relationship between PFS and CCAS

Incidence

Risk Factors

Anatomy

Pathophysiology

Prognosis

Treatment

Prevention

Statistical Analysis of 257 Pediatric Posterior Fossa Tumor Cases

Conclusion

Chapter 12. Functional Linguistic Topography of the Cerebellum

Introduction

Cerebellar Functional Topography: A Brief Overview

The Linguistic Topography of the Cerebellum

Conclusion

Chapter 13. Deep Cerebellar Nuclei (DCN) and Language

Introduction

Involvement DCN in Cognitive Functions

DCN and Language

Discussion

Conclusion

Chapter 14. The Use of Transcranial Magnetic Brain Stimulation to Study Cerebellar Language Function

Types of Brain Stimulation

What Has Been Found?

Some Outstanding Questions

Methodological Issues

Summary

Chapter 15. Experimental Use of Transcranial Direct Current Stimulation (tDCS) in Relation to the Cerebellum and Language

Introduction to Transcranial Direct Current Stimulation

Effects of Transcranial Direct Current Stimulation

Transcranial Direct Current Stimulation as a Performance Enhancer

Health and Safety in Transcranial Direct Current Stimulation

Cerebellar Transcranial Direct Current Stimulation

What Is Stimulated in Cerebellar Transcranial Direct Current Stimulation?

Are Cerebellar Transcranial Direct Current Stimulation Effects Polarity-Specific?

Cerebellar Transcranial Direct Current Stimulation and Language

Advantages of Cerebellar Transcranial Direct Current Stimulation over Functional Magnetic Resonance Imaging in Language Research

Advantages of Cerebellar Transcranial Direct Current Stimulation over Patient Studies in Language Research

Cerebellar Transcranial Direct Current Stimulation versus Repetitive TMS in Language Research

Evidence on Cerebellar Transcranial Direct Current Stimulation Effects on Language Processing

Predictions on Cerebellar Transcranial Direct Current Stimulation on Language Processing

Conclusion

Index

Copyright

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Contributors

Hermann Ackermann,     Department of Neurology and Stroke, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany

Michael Adamaszek,     Department of Neurologic and Cognitive Rehabilitation, Bavaria Clinic Kreischa, Kreischa, Germany

Louise Allen-Walker,     School of Psychology, Bangor University, Wales, UK

Georgios P.D. Argyropoulos,     Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, London, UK

Lauren A. Barker,     The Chicago School of Professional Psychology, Loyola University Chicago, Chicago, IL, USA

Lisa Bartha-Doering,     Department of Pediatrics and Adolescent Medicine, Medical University Vienna, Vienna, Austria

Alan A. Beaton

Department of Psychology, Aberystwyth University, Wales, UK

Department of Psychology, Swansea University, Wales, UK

Florian Bodranghien,     Laboratoire de Neurologie Expérimentale–ULB, Brussels, Belgium

R. Martyn Bracewell

School of Psychology, Bangor University, Wales, UK

School of Medical Sciences, Bangor University, Wales, UK

Hyo-Jung De Smet,     Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

John E. Desmond,     Departments of Neurology, Neuroscience and Cognitive Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA

Thora Gudrunardottir,     Oncological Department, Hilleroed Hospital, Copenhagen, Denmark; Posterior Fossa Society

Christophe Habas,     Service de NeuroImagerie, Hôpital des Quinze-Vingts, Université Pierre et Marie Curie, Paris, France

Ingo Hertrich,     Department of Neurology and Stroke, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany

Laura Jansons,     Private Practice, Arlington Heights, IL, USA

Kenneth C. Kirkby,     Department of Psychiatry, School of Medicine, University of Tasmania, Hobart, Australia

Leonard F. Koziol,     Private Practice, Park Ridge, IL, USA

Maria Leggio

I.R.C.C.S. Santa Lucia Foundation, Rome, Italy

Department of Psychology Sapienza University of Rome, Rome, Italy

Mario Manto,     Unité d’Etude du Mouvement, Université Libre de Bruxelles, Brussels, Belgium; Université de Mons, Mons, Belgium

Peter Mariën

Department of Neurology and Memory Clinic, ZNA Middelheim General Hospital, Antwerp, Belgium

Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

Cherie L. Marvel,     Departments of Neurology and Psychiatry, Johns Hopkins University School of Medicine, Baltimore, MD, USA

Klaus Mathiak

Department of Psychiatry, Psychotherapy and Psychosomatics, University Hospital Aachen, RWTH Aachen University, Aachen, Germany

Jülich-Aachen Research Alliance, JARA-Brain, Jülich, Germany

Marco Molinari,     I.R.C.C.S. Santa Lucia Foundation, Rome, Italy

Philippe Paquier

Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

Department of Neurology and Neuropsychology, University Hospital Erasme, ULB, Brussels, Belgium

Unit of Translational Neurosciences, School of Medicine and Health Sciences, Universiteit Antwerpen, Antwerp, Belgium

Jeremy D. Schmahmann,     Ataxia Unit, Cognitive Behavioral Neurology Unit, Laboratory for Neuroanatomy and Cerebellar Neurobiology, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA

Catherine J. Stoodley,     Department of Psychology and Center for Behavioral Neuroscience, American University, Washington, DC, USA

Kim van Dun,     Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

Dorien Vandenborre,     Cepos, Rehabilitation Centre, Rooienberg, Duffel, Belgium; Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium

Jo Verhoeven,     Language and Communication Science, City University London, Northampton Square, London, UK; Computational Linguistics & Psycholinguistics Research Center (CLiPS), University of Antwerp, Antwerp, Belgium

Wolfram Ziegler

EKN—Clinical Neuropsychology Research Group, Clinic for Neuropsychology, City Hospital Munich, Munich, Germany

Institute for Phonetics and Speech Processing, Ludwig-Maximilians-University Munich, Munich, Germany

Introduction

Peter Mariën¹,²,  and Mario Manto³,⁴,     ¹Department of Neurology and Memory Clinic, ZNA General Hospital, Middelheim, Antwerp, Belgium;,     ²Clinical and Experimental Neurolinguistics (CLIN), Vrije Universiteit Brussel, Brussels, Belgium,     ³Unité d’Etude du Mouvement, Université Libre de Bruxelles, Brussels, Belgium,     ⁴Université de Mons, Mons, Belgium

In less than three decades, the concept of cerebellar neurocognition has evolved from a mere afterthought to an entirely new and multifaceted area of neuroscientific research. A close interplay among three main strands of contemporary neuroscience has induced a substantial modification of the traditional view of the cerebellum as a simple coordinator of autonomic and somatic motor functions. Indeed, the wealth of currently available evidence derived from (1) detailed neuroanatomical investigations, (2) functional neuroimaging studies with healthy subjects and patients, and (3) in-depth neuropsychological assessment of patients with cerebellar disorders shows that the cerebellum plays also a cardinal role in affective regulation, cognitive processing, and linguistic functions. However, although considerable progress has been made in models of cerebellar function, controversy remains regarding the exact role of the linguistic cerebellum in a broad variety of nonmotor language processes.

This volume brings together a range of different viewpoints and opinions regarding the contribution of the cerebellum to language function. Recent developments and insights in the nonmotor modulatory role of the cerebellum in language and some related disorders are discussed by experts in the field. The role of the cerebellum in speech and language perception, in motor speech planning including apraxia of speech, in verbal working memory, in phonological and semantic verbal fluency, in syntax processing, in the dynamics of language production, in reading, and in writing will be addressed. In addition, the functional topography of the linguistic cerebellum and the contribution of the deep nuclei to linguistic function will be discussed. As such, with this volume, we hope to offer a framework for debate and discussion. The reader interested in the neuroscientific mysteries of this organ situated at the bottom of the brain will find not only state-of-the-art contributions, but also novel ideas that are being investigated in a growing number of laboratories worldwide. The fact that the cerebellum contains more neurons than any other region of the brain and is characterized by a geometrical structure makes it an excellent candidate for investigation of novel concepts in neuroscience.

Development of Concepts

Two centuries of research on cerebellar function have been dominated by the role of the cerebellum in motor control (see Manto et al., 2012 for a review). However, from time to time, clinical case descriptions and experimental evidence from animal studies dating back to the early part of the nineteenth century, already suggested an association between cerebellar pathology and a variety of nonmotor cognitive as well as affective dysfunctions (see Schmahmann, 1991, 1997). As early as 1831, Combettes described in the Bulletins de la Société Anatomique de Paris, the postmortem findings of an 11-year-old girl, Alexandrine Labrosse, who presented with neurodevelopmental disorders including a range of cognitive, affective, and motor impairments resulting from a complete absence of the cerebellum (Figure 1).

Nevertheless, a causal connection between cerebellar disease and cognitive and affective disturbances was dismissed for decades. In the mid-1900s, investigators started to examine a possible link between the cerebellum and cognition and emotion, exemplified by the work of Snider and Eldred (1948), Snider (1950), Snider and Maiti (1976), Dow (1974), Heath (1977, 1997), Heath, Franklin, and Shraberg (1979), Cooper, Riklan, Amin, and Cullinan (1978) and others (see Schmahmann, 1991 for a review). This laid a foundation for the rediscovery of this concept by Leiner, Leiner, and Dow (1986, 1991), who hypothesized that more recently evolved parts of the cerebellum contribute to learning, cognition, and language, and by Schmahmann (1991) and Schmahmann and Pandya (1987, 1989), who introduced the dysmetria of thought hypothesis (Schmahmann, 1998). These authors provided a historical, clinical, neuroanatomical, and theoretical framework within which a cerebellar role in higher cognitive and affective processes could be considered. That there may be a correlation between the size of the cerebellum and aspects of general intelligence has been known for some time (e.g., Allin et al., 2001; Ciesielski, Harris, Hart, & Pabst, 1997; Mostofsky et al., 1998; Paradiso, Andreasen, O’Leary, Arndt, & Robinson, 1997). From an evolutionary perspective, MacLeod, Zilles, Schleicher, Rilling, and Gibson (2003) demonstrated a reliable linear regression contrast between volumes of whole brain, cerebellum, vermis, and hemisphere of hominoids and monkeys and a striking increase in the lateral cerebellum in hominoids (Beaton & Mariën, 2010). After controlling statistically for age and sex, Pangelinan et al. (2011) showed with school-aged children that total cerebellar volume correlates significantly with cognitive ability (as measured by overall intelligence quotient) (but see Parker et al. (2008) for negative findings). Posthuma et al. (2003) reported that cerebellar volume in healthy adults (as well as total cerebral grey and white matter volumes) correlates with working memory performance. Such findings make it difficult to deny that the cerebellum is an organ of cognition (Justus & Ivry, 2001).

Figure 1  Early description by Combettes (1831) of an 11-year-old girl with a complex of cognitive, affective and motor developmental disturbances due to agenesis of the cerebellum.

Schmahmann Syndrome

Only a few years after the introduction of the dysmetria of thought theory, Schmahmann and Sherman (1998) described in a seminal study of patients with focal cerebellar lesions a consistent pattern of cognitive and affective deficits and coined the term cerebellar cognitive affective syndrome to describe this condition. Schmahmann syndrome, the eponym of cerebellar cognitive affective syndrome (Manto & Mariën, 2015), was characterized as a cluster of multimodal disturbances including: (1) executive deficits (deficient planning, set-shifting, abstract reasoning, working memory, and decreased verbal fluency), (2) disruption of visuospatial cognition (visuospatial disorganization and impaired visuospatial memory), (3) personality changes (flattening or blunting of affect, and disinhibited or inappropriate behavior), and (4) a range of linguistic impairments among which were dysprosodia, agrammatism, and mild anomia. However, analysis of the clinical data revealed that not all deficits occurred in each patient, but that certain symptoms were particularly prominent. Decreased verbal fluency, which did not relate to dysarthria, was said to be present in 18 of the 20 patients. Visuospatial disintegration, mainly consisting of disruption of the sequential approach to drawing and conceptualization of figures was found in 19 cases. Eighteen of the 20 patients presented with executive dysfunctions involving working memory, motor, and mental set-shifting and perseverations of actions and drawing. In 15 patients, frontal-like behavioral and affective changes were evident. Flattening of affect or disinhibition occurred, taking the form of overfamiliarity, flamboyant and impulsive actions, and humorous but inappropriate comments. Behavior was characterized as regressive and child-like in some cases and obsessive–compulsive traits were occasionally observed. Deficits in mental arithmetic were evident in 14 patients. Visual confrontation naming was impaired in 13 patients. Eight patients developed abnormal prosody characterized by high-pitched, whining, and a hypophonic speech quality. Mnestic deficits (verbal and visual learning and recall) were observed in some cases. The cluster of symptoms defining Schmahmann syndrome was associated with a decrease of general intellectual capacity. From an anatomoclinical perspective, cognitive and affective impairments were more prominent and generalized in patients with large, bilateral, or pancerebellar disorders, especially in a context of an acute onset of cerebellar disease. Posterior lobe damage was particularly important in the genesis of this novel syndrome. Damage of the vermal regions was consistently present in patients with disruption of affect. Anterior lobe damage was found to be less important to cause cognitive and behavioral deficits. Schmahmann syndrome in patients with stroke improved over time, but executive function remained abnormal. Schmahmann and Sherman (1998) pointed out that on the basis of their observations, it was not possible to distinguish the contribution of the lesioned cerebellum to these abnormal behaviors from that of the cerebral regions newly deprived of their connections with the cerebellum. Indeed, the clinical features of the cognitive and affective impairments constituting Schmahmann syndrome are identical to those usually identified in patients with supratentorial lesions affecting the cortical association areas and paralimbic regions and their interconnections. Reciprocal connections linking the cerebral association areas and paralimbic regions with the cerebellum constitute the neuroanatomical basis to explain the pathophysiological mechanisms of the cerebellar induced cognitive and affective deficits. As pointed out by Schmahmann and coworkers in an influential series of neuroanatomical studies, the cerebrocerebellar anatomical circuitry consists of a feedforward limb (the corticopontine and pontocerebellar pathways) and a feedback limb (the cerebellothalamic and thalamocortical systems) reciprocally connecting the cerebellum with the supratentorial regions crucially implicated in cognitive and affective processing. Since then, cerebellar involvement in linguistic processes has been studied by advanced neuroimaging methods in healthy subjects and several studies have been published focusing on a variety of linguistic dysfunctions following cerebellar lesions of different etiologies in children as well as adults. Reviews of the role of the cerebellum in nonmotor language functions are provided by Gordon (1996), Mariën, Engelborghs, Fabbro, and De Deyn (2001), Mariën et al. (2014), Paquier and Mariën (2005), De Smet, Baillieux, De Deyn, Mariën, and Paquier (2007), Beaton and Mariën (2010), Murdoch (2010), Highnam and Bleile (2011) and De Smet, Paquier, Verhoeven and Mariën (2013).

With the introduction of Schmahmann syndrome, neuroscientists dealing with the cerebellum have now a better idea of the topography of cerebellar deficits. Maps of lesion symptoms have been identified, clarifying the roles of cerebellar lobules in motor, cognitive, or behavioral operations.

The Subserving Neural Network

The neuroanatomical substrate of the recently acknowledged nonmotor role of the cerebellum in cognitive and affective processing is a dense and reciprocal network of crossed cerebrocerebellar pathways consisting of corticopontocerebellar and cerebellothalamocortical loops that establish a close connection between the cerebellum and the supratentorial motor, paralimbic, and association cortices subserving cognitive and affective processes. Several contemporary lesion-behavior and neuroimaging studies have demonstrated that, in addition to its somatotopic organization for motor control, the human cerebellum is topographically organized for higher order cognitive and affective functions as well. A meta-analysis of neuroimaging studies investigating cerebellar involvement in motor, cognitive, and affective processing paradigms has provided support for a dichotomy between the sensorimotor cerebellum—geographically organized in distinct regions in the anterior lobe—and the neurocognitive and affective cerebellum—represented in distinct parts in the posterior lobe (for a review, see Stoodley & Schmahmann, 2009). In addition, the majority of anatomoclinical studies of patients with linguistic impairments following focal cerebellar lesions and the majority of neuroimaging studies employing nonmotor language tasks typically show a lateralized involvement of lateral, posterior cerebellar regions (including lobules VI and Crus I/II) in nonmotor linguistic processes. Indeed, the patterns of lateralized (or even bilateral) cerebral representation of language in dextrals and sinistrals seem to be reflected at the cerebellar level by a lateralized linguistic cerebellum, subserved by crossed cerebellocerebral connections between the cortical language network and the cerebellum.

The Theoretical Foundation

The theory that the cerebellum operates as an essential modulator of higher level cerebral functions, including language and affect, currently attracts much attention of the scientific community, yet no consensus exists about the exact role and contributions of the cerebellum to the cognitive and affective domain. Because of its uniform neuroanatomical structure and its dense connections with the supratentorial association areas via cerebrocerebellar pathways (corticopontine-pontocerebellar-cererebellothalamic-thalamocortical), the cerebellum is considered a functional entity that contributes in a unique and general way to information processing (universal cerebellar transform; Schmahmann, 2000, 2001, 2004, 2010; Stoodley & Stein, 2013). One of the computational models that supports this view on integrated cerebellar motor, cognitive, and affective function is the dysmetria of thought theory that regards the cerebellum as an oscillation dampener (realizing a maintenance of functioning around a homeostatic baseline, to smooth out performance in all domains: cognitive, motor, and emotional) (Schmahmann, 2000, 2001, 2004, 2010). Several authors (Courchesne & Allen, 1997; Desmond, Gabrieli, Wagner, Ginier, & Glover, 1997; Stoodley & Stein, 2013) regard the computational contribution of the cerebellum to motor, cognitive, and affective function as a predictor of future states. This functional role implicates that the cerebellum generates internal neural forward models by means of optimization of motor programs and mediation of cognitive functioning. In a number of studies, Ito (2008) suggested that the corticonuclear microcomplexes of the cerebellum function as learning machines, performing a comparator role consisting of the formation and updating of internal models through error learning (error predictions, processing, and correction). According to others, the cerebellum may act as an internal clock crucially involved in the detection of deviations of an expected timing (control and regulation of motor and cognitive functions) (Ivry, 1997; Ivry, Spencer, Zelaznik, & Diedrichsen, 2002) or as a detector of change and deviations of sequential events (Ackermann, 2008; Leggio, Chiricozzi, Clausi, Tedesco, & Molinari, 2011; Molinari, Chiricozzi, Clausi, Tedesco, De Lisa, & Leggio, 2008; Stoodley et al., 2009; Stoodley, Valera, & Schmahmann, 2011). In other studies, the role of the cerebellum is described as a control mechanism of shifts of attention, priming and boosting activity in the extracerebellar system to operate rapidly and efficiently (Courchesne & Allen, 1997; Salmi et al., 2009). More research is needed to elucidate the theoretical underpinnings of cerebellar neurocognition. An integrated vision of the theoretical conceptualizations of the general contribution of the cerebellum in cognitive functioning might be that of a high-level operational device that does not subserve a specific cognitive or affective function in itself but rather lends an active support to the central processes in a variety of ways including prediction of the consequences of a motor, affective or cognitive action or by error detection (in a sequence or in time).

The primary goal of this volume is to collect and summarize the key concepts that have been proposed to explain the role of the cerebellar circuits in linguistic processing. To this aim, we have gathered contributions from several leading experts in various areas of cerebellar language processing, providing a range of different, sometimes even controversial, viewpoints. As demonstrated in this book, several dimensions of speech and language production and perception seem to depend upon the modulatory role of the cerebellum: phonetic timing operations, auditory signal segregation and cross-modal binding mechanisms, adaptive sensorimotor function of speech motor planning, articulatory control processes in verbal working memory, nonautomatic sequence strategies in verbal fluency, temporal coordination and recall of established explicit internal representations of sentence structures, high-level language functions (e.g., figurative language, word association, antonym/synonym generation), planning and execution of manual production of letters, and reading (development). Nonmotor linguistic function of the human cerebellum seems to be topographically organized in a lateralized linguistic cerebellum which reflects the patterns of cerebral language dominance in dextrals and sinistrals. In the majority of dextrals the lateralized linguistic cerebellum comprises, the right ventrocaudal part of the dentate nucleus and the right posterior lateral cerebellum (involving lobules VI–VIII) that is reciprocally linked to the supratentorial language networks of the dominant hemisphere. However, anatomical studies providing direct evidence of reciprocal cerebellar connections to language areas are still lacking. Although final agreement has not yet been reached, we believe that a new consensus that draws on and integrates the ideas presented here will eventually emerge to unravel the enigmatic role of the cerebellum in nonmotor linguistic processing. At a time where the field of ataxiology is being refined and keeps growing in popularity, it is our hope that readers will find this book informative and useful.

We are particularly grateful to all the contributors who have found time to prepare excellent chapters despite a busy schedule. We are thankful to the anonymous reviewers for their constructive input and the staff of Elsevier for their permanent support in the preparation of this book.

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Chapter 1

The Phonetic Cerebellum

Cerebellar Involvement in Speech Sound Production

Wolfram Ziegler¹,²     ¹EKN—Clinical Neuropsychology Research Group, Clinic for Neuropsychology, City Hospital Munich, Munich, Germany     ²Institute for Phonetics and Speech Processing, Ludwig-Maximilians-University Munich, Munich, Germany

Abstract

Tying in with theories postulating that the cerebellum contributes not only to motor coordination but also to cognitive and emotional processing, this chapter seeks to identify the role of the cerebellum in the processing hierarchy from phonological encoding to motor planning and motor execution and in the emotional and attitudinal modulation of speech output. In a first section, neuroanatomical evidence for an implication of the cerebellum on each of the four different stages is discussed. In a second section, the clinical patterns of sound production impairment after cerebellar lesions are reviewed. The existing data, predominantly the clinical evidence, point at an implication of the cerebellum in motor execution and motor activation, but not in phonetic planning (motor programming) and phonological encoding. It is concluded that at the linguistic level of speech sound production, the contribution of the cerebellum is essentially restricted to lower level motor control and basic motor activation processes.

Keywords

Ataxic dysarthria; Cerebellum; Connectivity; Motor activation; Motor coordination; Motor planning; Phonology; Speech apraxia; Topography

Introduction

The processes dealing with the production of speech sounds for words and sentences are commonly broken down into several subcomponents. Depending on which theoretical framework is chosen, different processing stages are distinguished. A prominent psycholinguistic model developed by Levelt, Roelofs, and Meyer (1999), for instance, makes a distinction between four discrete processing steps by which (1) word forms are retrieved from a mental lexicon, (2) the phonemes constituting a word are mapped onto the word’s rhythmical frame (phonological encoding), (3) motor plans are retrieved for syllabified phonological forms (phonetic planning), and (4) these motor plans are implemented in the neuromuscular system controlling speech movements (articulation). Otherwise, models focusing on the lower levels of speech production are less elaborate regarding abstract lexical and phonological processes, but are more concerned with control subsystems of the speech motor apparatus (e.g., Guenther, Ghosh, & Tourville, 2006; Hickok, 2014). Clinically, distinctions between different stages of speech production are reflected in a widely accepted taxonomy of neurogenic speech sound disorders, with a classification into lexical and postlexical phonological impairments (Schwartz, 2014), motor planning impairment (apraxia of speech; cf. Ziegler, Aichert, & Staiger, 2012), motor execution disorders (dysarthria; cf. Duffy, 2013), and impairments of motivational or emotional aspects of speaking and speech initiation (Ackermann & Ziegler, 2010).

Assuming that different parts of the brain are engaged in the different processing stages translating stored word forms into fully specified articulatory-motor patterns, the question that is pertinent in this volume is whether there is a contribution of the cerebellum to speech sound production on one or several of these stages and how this contribution can be framed in theories of speech production. Conventionally, a major (and undisputed) role of the cerebellum in speech is seen in the sensorimotor control and coordination of vocal tract and laryngeal and respiratory movements during spoken language production (Ackermann, 2008). In this vein, speech impairment after cerebellar lesions has been characterized as a dysarthria syndrome, more specifically as ataxic dysarthria (Kent et al., 2000). This perspective is consistent with the traditional understanding of the cerebellum as an organ that is primarily engaged in the coordination of movement (Holmes, 1917) and the processing of sensory information during online motor control (Gao et al., 1996).

Yet, along with a general revision of this view and with the discovery of significant cerebellar contributions to linguistic, cognitive, and affective processing (Schmahmann, 1991), the understanding of the cerebellum as a purely sensorimotor coordination organ in speaking has been challenged (Marien, Engelborghs, Fabbro, & De Deyn, 2001). An extensive number of studies exists focusing on such higher order functions, both in the functional imaging (e.g., Keren-Happuch, Chen, Ho, & Desmond, 2014) and the clinical domain (Stoodley & Schmahmann, 2009a), and consensus papers wrapping up the major findings have been published recently (Koziol et al., 2014; Manto et al., 2012; Mariën et al., 2014). As commented by Schlerf, Wiestler, Verstynen, and Diedrichsen (2014, p. 199), the cerebellum appears to play a role in nearly as many separate functions as the neocortex.¹

Regarding the production of spoken language, this raises the question as to whether the cerebellum has a role beyond the motor coordination of the speech organs (i.e., whether it is also engaged in higher level processes of speech sound production such as phonological encoding, phonetic planning, or the motivational and affective modulation of speech). In this chapter, existing evidence on motor, linguistic, and emotional functions of the cerebellum will be reviewed from the perspective of how they may contribute to speech production, from the phonological to the motor execution and activation level.

Cerebellar Contributions to Speech: Neuroanatomical Basis

The understanding that the human cerebellum is an organ whose functions are not limited to the coordination of movement is supported by new evidence about its topographic organization and its connectivity with distinct motor and nonmotor areas of the cerebral cortex (Stoodley & Schmahmann, 2010). Because many of these data stem from anatomical investigations in nonhuman primates, careful interpretation is warranted when it comes to speech and language because monkeys and apes do not speak and because the contribution of the cerebellum to precursor functions of speech in these animals has not been examined extensively.

The Role of the Cerebellum in Nonhuman Primate Vocalizations

The vocalizations of nonhuman primates are considered, by some researchers, as a possible precursor of human speech (for references cf. Ackermann, Hage, & Ziegler, 2014; Ackermann & Ziegler, 2010). Nonetheless, surprisingly little is known about the role of the cerebellum in vocal communication in our closest living relatives. Larson, Sutton, and Lindeman (1978) examined rhesus monkeys which were trained to emit specific coo vocalizations. Experimental lesions applied to the cerebellar nuclei and a partial removal of the cerebellar cortex produced inconsistent changes in average fundamental frequency and/or loudness and/or duration of the conditioned coo calls in some, but not all, of the five animals. Unlike animals with lesions to mesiofrontal cerebral cortex (anterior cingulate gyrus), monkeys with cerebellar lesions did not decrease their call frequency. Larson et al. (1978) therefore concluded that the cerebellum is involved in the modulation of pitch and loudness, but not in call initiation or the modulation of the impulse to vocalize. Of note, however, the vocal alterations mentioned in this study had nothing in common with the voice impairments observed in humans with cerebellar dysfunctions (see the following section). In a later study by Kirzinger (1985), experimental bilateral destruction of the cerebellar nuclei of three squirrel monkeys had no effect on electrically induced conspecific vocalizations in these animals, although their limb movements became severely ataxic. Contrasting her results with those described by Larson et al. (1978), Kirzinger (1985, p. 180) speculated that the cerebellum may play a role in the volitional recruitment of the larynx for vocal communication and the regulation of the unspecific arousal level underlying vocalization in nonhuman primates, but not in the coordination of laryngeal movements.

By conclusion, these data do not provide clear evidence that the (nonhuman) primate cerebellum may serve as a model of human cerebellar function in speaking. As a side note: In songbirds, which are considered to constitute an important animal precursor model of especially the vocal imitation and vocal learning aspects of human speech, there is also no evidence so far of any significant contribution of the avian homologue of the cerebellum to birdsong (Ackermann & Ziegler, 2013). Therefore, speculating about the possible specificity of a cerebellar contribution to vocal communication in our species, Ackermann (2008, p. 269)claimed that during hominine evolution expression of the human-specific variant of the FOXP2 gene created a permissive environment within the primate cerebellar motor circuit through which the extant motor computational resources of the cerebellum could be harnessed for the vocal apparatus in the generation of the sequential motor patterns involved in articulation (for a similar argument relating to the basal ganglia, see Ackermann et al., 2014).

Topographic Organization and Connectivity of the Human Cerebellum From a Speech Perspective

Although current knowledge about the topography and connectivity of the human cerebellum has to a large part been inferred from transneural tract tracing studies in nonhuman primates (for a review, see Schmahmann, 2010), more recent studies using new in vivo diffusion tractography techniques have added evidence on cerebrocerebellar connectivity in the intact human brain that is by and large compatible with animal data (Catani & Thiebaut de Schotten, 2008; Granziera et al., 2009).

In earlier anatomical models, the cerebellum was considered a motor organ that funnels afferent information from different regions of the cortex into output channels targeted primarily at the motor cortex. Modern theories, in contrast, assume that the cerebellum communicates through several parallel closed-loop circuitries with motor, associative, and paralimbic cortical areas of the large brain (Krienen & Buckner, 2009; Ramnani, 2006; Stoodley & Schmahmann, 2010; Strick, Dum, & Fiez, 2009). It is claimed that through this arrangement the cerebellum is implicated not only in sensorimotor, but also in cognitive, linguistic, and affective functions.

The Motor Cerebellum

Among the 10 lobules that are distinguished within the cerebellar cortex, those pertaining to the anterior lobe (lobules I–V) as well as lobule VIII and parts of lobule VI of the posterior lobe are considered predominantly sensorimotor. Hemispheric lobule VI is particularly relevant here because it contains the lip and tongue area of a sensorimotor homunculus (Mottolese et al., 2013). However, early electrophysiological investigations in animals and more recent functional imaging studies in humans have revealed that there is at least one further cerebellar homunculus in the posterior lobe, with a tongue area located in lobule VIII, but still other somatotopic maps (i.e., no less than four homunculi) are considered to exist in the anterior and posterior lobes (Buckner, Krienen, Castellanos, Diaz, & Yeo, 2011; Grodd, Hülsmann, Lotze, Wildgruber, & Erb, 2001; Manni & Petrosini, 2004; Rijntjes, Büchel, Kiebel, & Weiller, 1999; Schlerf et al., 2010).

From animal work, it is known that the cerebellar cortical face areas in lobule VI receive somatosensory afferent information from oral and facial muscles via the trigeminal nuclei through the inferior cerebellar peduncles (Stoodley & Schmahmann, 2010, p. 832). This afferent input is considered to provide the cerebellar cortex with information about the sensory state of the speech organs. Furthermore, the cerebellar hemispheres receive afferent projections travelling through pontine nuclei from motor areas of the contralateral cerebral cortex, especially from primary motor cortex, ventral premotor cortex, and supplementary motor area (Brodal, 1978; Glickstein, May, & Mercier, 1985; Schmahmann, Rosene, & Pandya, 2004).² These projections are somatotopically organized throughout their pathway to the nuclei in the basis pontis and further on through primarily the contralateral middle cerebellar peduncle to the cerebellum (for references cf. Ramnani, 2006; Stoodley & Schmahmann, 2010). From there, efferent fibers travel through output channels in the deep cerebellar nuclei to the motor-nuclei of the contralateral thalamus and back to the motor areas of the cerebral cortex, still in a somatotopically organized fashion (Middleton & Strick, 2000). Hence, the motor cerebellum is connected with cerebral motor cortical areas via a two-stage feedforward limb through the basis pontis and via a two-stage feedback limb through the thalamus (e.g., Kelly & Strick, 2003). Several spatially distinct, somatotopically organized loops are considered to project back to the primary motor, ventral premotor, and supplementary motor areas from which they originate, thereby forming separate closed feedforward-feedback motor circuits. Apart from these dentate-thalamico-cerebral feedback projections, Mottolese et al. (2013) inferred from electromyographic latencies obtained during direct perioperative mapping in humans that efferent cerebellar signals effectuate motor responses not via a cerebral cortical feedback loop, but rather more directly through a descending subcortical cerebelloreticular pathway.

By analogy to limb motor control, the described system constitutes the substrate of the contribution of the cerebellum in oral motor control and motor speech. A rather specific cerebellar mechanism in speech motor control was disclosed by Golfinopoulos et al. (2011), who performed a jaw-perturbation experiment in the functional magnetic resonance imaging (fMRI) scanner to examine the neural substrate of somatosensory feedback control. Increased activation in bilateral lobule VIII was found in perturbed versus unperturbed speech, which was interpreted as an indication that this region facilitates somatosensory cortex in the monitoring and correction of unexpected perturbations in the periphery.

The data described so far leave several unanswered questions, such as (1) whether the motor loop involving the vocal tract and laryngeal muscles in humans is lateralized for speech motor control; (2) whether the cerebrocerebellar motor system composes two separate loops, one