The Linguistic Cerebellum

427 Pages·2016·9.929 MB·English

by  Manto, Mario, Mariën, Peter

THE LINGUISTIC
CEREBELLUM
Edited by
PETER MARIËN
Department of Neurology and Memory Clinic, ZNA
Middelheim General Hospital, Antwerp, Belgium; and
Clinical and Experimental Neurolinguistics (CLIN), Vrije
Universiteit Brussel, Brussels, Belgium
and
MARIO MANTO
Unité d’Etude du Mouvement
Université Libre de Bruxelles,
Brussels, Belgium; and Université de
Mons, Mons, Belgium
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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
xi
xii Contributors
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
Contributors xiii
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, 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 multifac-
eted area of neuroscientific research. A close interplay among three main
strands of contemporary neuroscience has induced a substantial modifi-
cation of the traditional view of the cerebellum as a simple coordinator
of autonomic and somatic motor functions. Indeed, the wealth of cur-
rently 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 opin-
ions 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 ver-
bal 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
xv
xvi Introduction
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 experi-
mental 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 dysfunc-
tions (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 neurode-
velopmental 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 cogni-
tive 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 theoreti-
cal framework within which a cerebellar role in higher cognitive and affec-
tive 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 regres-
sion 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
Introduction xvii
statistically for age and sex, Pangelinan et al. (2011) showed with school-
aged children that total cerebellar volume correlates significantly with cog-
nitive ability (as measured by overall intelligence quotient) (but see Parker
et al. (2008) for negative findings). Posthuma et al. (2003) reported that
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 cerebel-
lum.
cerebellar volume in healthy adults (as well as total cerebral grey and white
matter volumes) correlates with working memory performance. Such find-
ings make it difficult to deny that the cerebellum is “an organ of cognition”
(Justus & Ivry, 2001).
xviii Introduction
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 ver-
bal fluency), (2) disruption of visuospatial cognition (visuospatial disorganiza-
tion 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 promi-
nent. Decreased verbal fluency, which did not relate to dysarthria, was said to
be present in 18 of the 20 patients. Visuospatial disintegration, mainly consist-
ing 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 disinhi-
bition occurred, taking the form of overfamiliarity, flamboyant and impulsive
actions, and humorous but inappropriate comments. Behavior was character-
ized 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, whin-
ing, and a hypophonic speech quality. Mnestic deficits (verbal and visual learn-
ing 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 impair-
ments were more prominent and generalized in patients with large, bilateral,
or pancerebellar disorders, especially in a context of an acute onset of cerebel-
lar 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
Introduction xix
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 contribu-
tion 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 consti-
tuting 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 link-
ing the cerebral association areas and paralimbic regions with the cerebellum
constitute the neuroanatomical basis to explain the pathophysiological mech-
anisms of the cerebellar induced cognitive and affective deficits. As pointed
out by Schmahmann and coworkers in an influential series of neuroanatomi-
cal 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 cogni-
tive 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 lin-
guistic dysfunctions following cerebellar lesions of different etiologies in chil-
dren 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 deal-
ing with the cerebellum have now a better idea of the topography of cere-
bellar 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,