Handbook of Clinical Neurology, Vol.

154 (3rd series)

The Cerebellum: From Embryology to Diagnostic Investigations
M. Manto and T.A.G.M. Huisman, Editors
https://doi.org/10.1016/B978-0-444-63956-1.00011-4
Copyright © 2018 Elsevier B.V. All rights reserved

Chapter 11

Language and the cerebellum

PETER MARIËN1* AND RENATO BORGATTI2
1
Clinical and Experimental Neurolinguistics, Free University of Brussels, Brussels, Belgium
2
Department of Neuropsychiatry and Neurorehabilitation Unit, Eugenio Medea Scientific Institute, Bosisio Parini, Lecco, Italy

Abstract
During the past decades neuroanatomic, neuroimaging, and clinical studies have substantially changed the
long-standing view of the role of the cerebellum as a sole coordinator of sensorimotor function. Currently,
the cerebellum is considered to be crucially implicated in a variety of cognitive, affective, social, and
behavioral processes as well.
In this chapter we aim to summarize a number of critical insights from different research areas (neu-
roanatomy, functional neuroimaging, clinical practice) that provide evidence for a role of the cerebellum in
motor speech and nonmotor language processing in both adults and children.
Neuroanatomic studies have provided a robust basis for the development of new insights in the modulatory
role of the cerebellum in neurocognition, including nonmotor language processing by means of identifying
a dense network of crossed reciprocal connections between the cerebellum and the supratentorial association
areas. A topologic distinction has been established between the “motor” cerebellum, projecting to the cortical
motor areas, and the “cognitive/affective” cerebellum, connected with the cortical and limbic association
areas. Neuroimaging studies have demonstrated cerebellar involvement in several different language tasks,
even after controlling for motor aspects. In addition, several clinical studies have identified a variety of
nonmotor linguistic deficits after cerebellar disease in both children and adults, implying a prominent role
for the cerebellum in linguistic processes. Functional neuroimaging has confirmed the functional impact
of cerebellar lesions on remote, structurally intact cortical regions via crossed cerebellocerebral diaschisis.
Overall, evidence from neuroanatomic, neuroimaging, and clinical studies shows a (strongly latera-
lized) involvement of the cerebellum in a broad spectrum of nonmotor language functions through a dense
network of crossed and reciprocal cerebellocerebral connections. It is argued that the cerebellum is
involved in language in a similar manner as it is involved in motor functions: through monitoring/
coordinating cortical functions via timing and sequencing mechanisms.

INTRODUCTION
The role of the cerebellum has been considered for two
centuries to consist solely of pure sensorimotor control
(Manto and Mariën, 2015). Over the last few decades,
however, cumulative evidence from neuroanatomic, neu-
rophysiologic, neuroimaging, and clinical studies has
changed this view substantially. A huge number of studies
support the view that the cerebellum plays a prominent
role in cognitive, affective, and behavioral functions,
including nonmotor language functions (De Smet et al.,
2013; Mariën et al., 2014). In this chapter, we concisely
review the rapidly growing evidence derived from a
number of neuroanatomic, neurophysiologic, neuroim-
aging, and clinical studies to demonstrate the crucial
involvement of the cerebellum in a wide variety of nonmo-
tor linguistic processes. In addition, current hypotheses
about the possible underlying pathophysiologic and cog-
nitive mechanisms will be briefly discussed.

*Correspondence to: Professor Dr. Peter Mariën, Department of Neurology and Memory Clinic, ZNA AZ Middelheim, Lindendreef 1,
B-2020 Antwerp, Belgium. Tel: +32-3-280-31-36, E-mail: peter.marien5@telenet.be
182 P. MARIËN AND R. BORGATTI
EVIDENCE FOR A ROLE FOR THE
CEREBELLUM IN LANGUAGE
Anatomic
Neuroanatomically the cerebellum is not only densely
interconnected with the supratentorial motor areas, but
also with the paralimbic and association cortices through
a network of reciprocal crossed cerebellocerebral
pathways (Strick et al., 2009; Ramnani, 2012). The cer-
ebellum receives input from the cerebral cortical regions
via corticopontocerebellar projections, while feedback
is provided via cerebellothalamocortical projections
(Mariën et al., 2014). Histologic tract-tracing studies in
monkeys have shown that these feedforward and feed-
back projections form closed loops: a cerebellar area
projects back to the cortical areas, from which it receives
input (Strick et al., 2009) (Fig. 11.1).
In addition, neuroanatomic and neurophysiologic stud-
ies have identified a topologic distinction between a
"motor" and a "cognitive/affective” cerebellum. Motor-
related cortices project primarily to the contralateral
anterior cerebellar lobe (lobules I–V) -extending into
medial lobule VI, and to lobule VIII via the caudal
half of the pons. Prefrontal, parietal, and temporal
association areas project to the posterior cerebellar lobe
(crus I, crus II, lobule VI/VIIb/IX) via the mediorostral
(prefrontal areas) and dorso- and ventrolateral pons
(posterior cerebral hemispheres) (Habas et al., 2009;
Stoodley and Schmahmann, 2010; Keren-Happuch
et al., 2014; Mariën et al., 2014). The affective functions
are believed to be primarily situated in the cerebellar pos-
terior vermis (Stoodley and Schmahmann, 2009,2010;
De Smet et al., 2013) (Fig. 11.2).
This topographic division of the human cerebellum is
also supported by separate olivocerebellar connections,
forming olivocerebellar modules (see Chapter 3).
Whereas cutaneokinesthetic information is provided to
the cerebellum via spinocerebellar and trigeminocerebel-
lar tracts (with the medial and dorsal accessory olivary
nuclei projecting on the sensorimotor cerebellum (lob-
ules I–V, VI, VIII)), the principal olivary nucleus (with
little or no spinal cord input) is connected with lobule
VII and the dentate nucleus (DN), and to a smaller
degree with lobule VI (Stoodley and Schmahmann,
2010). A similar topographic division between motor
and nonmotor areas can also be found in the DN, the thal-
amus, and the pons, the areas involved in the reciprocal
cerebellocerebral loops (Fig. 11.1). Most of the output

CEREBELLUM MOTOR- ASSOCIATION

RELATED CORTEX
ncl. dentatus CORTICES PROJECTIONS
PONTINE
ncl.interpositus NUCLEI
ncl.fastigii Prefrontal Posterior Cerebral
fibers hemisphere

THALAMUS CAUDAL MEDIAL DORSAL/LATERAL

HALF OF ROSTRAL VENTRAL
PONS PONS PONTINE NUCLEI
‘MOTOR’ NUCLEI ‘NON-MOTOR’ NUCLEI
ncl. ventralis anterior intralaminar nuclei
ncl. ventralis intermedius ncl. medialis

CONTRALATERAL CONTRALATERAL
CORTEX CEREBELLAR CEREBELLAR
ANT.LOBE POST.LOBE
PREFRONTAL CINGULATE GYRUS
MOTOR
PRE-SMA PARAHIPPOCAMPAL
PREMOTOR
SUPERIOR TEMPORAL GYRUS
SMA PROPER
POSTERIOR PARIETAL LIMBIC CORTICES

A B
Fig. 11.1. (A) Diagram depicting the cerebellocerebral connectivity network underlying cognitive and affective processes. The
feedback or efferent loop originates from the deep nuclei of the cerebellum that project to the motor (gray arrows) and nonmotor
(blue arrows) nuclei of the thalamus. In turn, the motor nuclei of the thalamus project to motor and premotor cortices (gray arrows)
but also to nonmotor association cortices (blue arrows). The nonmotor nuclei of the thalamus project only to association cortices
(blue arrows). SMA, supplementary motor area. (Adapted from Mariën et al. (2013) with permission from Springer.) (B) Topo-
graphic distribution of motor-related cortices and association cortex feedforward or afferent projections to the cerebellum. Both
motor corticopontine projections and association cortex projections are somatotopically organized in the pons. (See also Stoodley
and Schmahmann (2010). Adapted from Grimaldi and Manto (2012) with permission from Springer.)
 LANGUAGE AND THE CEREBELLUM
anterior cerebellum
superior posterior lobe
inferior posterior
HIV
lobe
HV
HVI
HVII
crus I
HVII
crus II
HVIIb
HVIII
HIX
hemisphere
Fig. 11.2. Simplified representation of the dichotomy of the cerebellum in a motor (anterior) and a cognitive/affective (posterior/
vermis) cerebellum. (Adapted from Manto M, Mariën P (2015) Schmahmann’s syndrome – identification of the third cornerstone
of clinical ataxiology. Cerebellum Ataxias 2(1).)
and input of the lateral cerebellum is regulated by the
DN, and a division between a motor and a nonmotor
area is also found in the DN (Habas et al., 2015). Projec-
tions to and from the motor areas pass through the dorsal
part of the DN, while the projections from the associative
cortices pass through the ventral part of the DN (Strick
et al., 2009; Schlerf et al., 2014).
From an evolutionary point of view, the larger size
of the DN in humans than in primates is considered
the result of expansion of the ventrolateral “nonmotor”
part of the human DN (Matano, 2001). Enlargement of
the DN might reflect the increased importance of nonmo-
tor functions in humans (Strick et al., 2009), especially
since its development during evolution coincided with
the expansion of the prefrontal cortex (Middleton and
Strick, 1994, 2001). Leiner et al. (1986) suggested that
the parallel expansion of the ventral DN and the frontal
cortical areas, which are intrinsically implicated in cog-
nitive functioning, implies involvement of the cerebel-
lum in cognitive and linguistic processes as well. This
hypothesis is firmly endorsed by current insights in the
neuroanatomic projections from the ventral DN to the
prefrontal cortex.
Development
Cerebellar development follows a highly orchestrated
series of neurobiologic processes. Between 20 and
40 weeks of gestation and during the first few months
183
I
HII
HIII II
III MOTOR
IV
V
VI COGNITIVE
VIIa
VIIb
VIII
AFFECTIVE
IX
vermis
of life the cerebellum undergoes a rapid increase in
size, unparalleled by that of any other cerebral structure
(Limperopoulos et al., 2005; Clouchoux et al., 2012).
There is growing evidence to support a crucial role of
the cerebellum during early development, a period of
intense skill acquisition, for the optimization of both
structure and function in the developing cerebral cortex
(Limperopoulos et al., 2010; Wang et al., 2014; D’Mello
and Stoodley, 2015; Moberget et al., 2015; Stoodley and
Limperopoulos, 2016). While the association between
cerebellar structure and function and cognitive perfor-
mance in adults is consolidated through several studies,
during development this relationship is less clear and still
being defined. Emerging evidence from fetal, neonatal,
and pediatric populations supports the existence of a
regional functional topography of the cerebellum, and
provides testable hypotheses for clarifying the role of
the cerebellum in motor, cognitive, and social/behavioral
development (Limperopoulos et al., 2005; Clouchoux
et al., 2012; Stoodley and Limperopoulos, 2016). It is
well known that the cerebellum is involved in various
types of implicit/procedural learning (Timmann et al.,
2010), supporting new stages of representation through-
out cognitive development (Karmiloff-Smith, 1995). For
higher-level motor, cognitive, and behavioral tasks, the
cerebellum provides this modulatory function via cerebro-
cerebellar loops with sensorimotor, association, and lim-
bic regions of the cerebral cortex. In this way, the
cerebellum is well positioned to drive the optimization
184 P. MARIËN AND R. BORGATTI
of cerebral cortical circuits as skills are acquired and
made fluent throughout childhood and into adolescence
(Stoodley and Limperopoulos, 2016).
In addition, it has been suggested that the cerebellum
may have a crucial role in the optimization of both struc-
ture and function in the developing brain (Wang et al.,
2014; D’Mello and Stoodley, 2015; Stoodley and
Limperopoulos, 2016) and that it is involved in setting
up the specialization of cortical regions involved in
cognitive processes, with a crucial organizing effect dur-
ing development. This developmental pattern strongly
suggests the presence of a critical period for cerebellar
development, which is central to both the cerebellum’s
vulnerability and the developmental repercussions of
injury, which are capable of disrupting this highly regu-
lated, programmed developmental course.
Early cerebellar damage can lead to structural alter-
ations beyond the fetal and neonatal period, reflecting
the impact of an early cerebellar lesion on neural func-
tion. Structural neuroimaging studies show that the
reduction of both cerebrocerebellar white-matter path-
ways and the gray-matter volume of distal regions of
the cerebral cortex to which the cerebellum projects
supports the developmental diaschisis model proposed
by Wang and colleagues (2014).
Early disruption of the cerebellum, prenatal cerebellar
developmental lesions (i.e., malformations), cerebellar
posterior fossa tumors in early childhood, or neurodeve-
lopmental disorders lead to significant long-lasting and
wide-ranging changes in the structure and function of cer-
ebrocerebellar systems, with long-term effects. Cerebellar
damage earlier in life, due to compensatory plasticity,
can result in wide-ranging developmental (motor, cogni-
tive, linguistic, and behavioral) outcomes (Riva and
Giorgi, 2000; Scott et al., 2001; Limperopoulos et al.,
2007; Tavano et al., 2007a; Kirschen et al., 2008; Davis
et al., 2010; Stoodley and Limperopoulos, 2016).
Functional imaging
POSITRON EMISSION TOMOGRAPHY
In the late 1980s, Petersen et al. (1989) for the first time
identified right cerebellar activation in language task
experiments with positron emission tomography. In their
study the authors used three conditions: first, single
words were presented both aurally and visually to
17 right-handed healthy subjects without any action
required (sensory task), then they asked these subjects
to repeat the presented word (output task), and finally
they had to perform a noun–verb association task (associ-
ation task) in which an auditory-presented noun had to
be silently associated with a semantically related verb
(e.g., car – to drive). Activation of the right lateral inferior
cerebellum was found, specifically in the noun–verb
association task. Referring to the anatomic paper of
Leiner et al. (1986), the authors speculated that this acti-
vation rather had a “cognitive” role than a motor or a sen-
sory one (Petersen et al., 1989). Since this study, a large
number of experimental and clinical neuroimaging studies
have confirmed consistent involvement of the right poste-
rior cerebellum in silent word generation tasks (Martin
et al., 1995; Grabowski et al., 1996; Papathanassiou
et al., 2000) (Table 11.1).
FUNCTIONAL MAGNETIC RESONANCE IMAGING (FMRI)
Stoodley and Schmahmann (2009) performed an activa-
tion likelihood estimate meta-analysis including 11 fMRI
studies (performed between 1998 and 2006) to investigate
language-specific activations, controlled for motor acti-
vation. Several different language tasks were used and
contrasted with various motor tasks to isolate specific
language functions, such as phonologic and semantic pro-
cessing, and word generation. For all language tasks, the
strongest peaks in the analysis were lateralized in lobule VI,
crus I/II, and midline lobule VII of the right cerebellum.
Only a small lateral cluster was found in the left-hemisphere
lobule VI (Stoodley and Schmahmann, 2009).
A more recent meta-analysis performed by Keren-
Happuch et al. (2014) confirmed the activation of the right
lateral posterior cerebellum during language tasks. This
study specifically targeted cerebellar activation clusters.
Four studies were included in addition to the meta-analysis
of Stoodley and Schmahmann (2009), expanding the
range from 2006 to 2010 (Keren-Happuch et al., 2014).
Thus, involvement of the right posterior lateral cerebellar
hemisphere in language via crossed anatomic connections
with the language-dominant left frontal, parietal, and
temporal association areas was confirmed by functional
neuroimaging.
An fMRI study of Hubrich-Ungureanu et al. (2002)
also demonstrated crossed cerebellocerebral activations
subserved by crossed anatomic tracts between the
supratentorial association cortices and the cerebellum.
A right-handed subject with typical left-hemisphere lan-
guage dominance and a left-handed subject with atypical
right-hemisphere language dominance were asked to
silently perform a verbal fluency task in the MR scanner.
In addition to activation of the left frontoparietal cortex,
involvement of the right cerebellar hemisphere was
found in the right-handed subject, while in the left-handed
subject, the left cerebellar hemisphere was coactivated
with the right frontoparietotemporal cortex (Hubrich-
Ungureanu et al., 2002). This study not only confirmed
involvement of the cerebellum in language tasks, it also
showed a clear lateralization of cerebellar involvement
contralateral to the language-dominant left or right cere-
bral hemisphere (Mariën et al., 2001b).
Table 11.1
Overview of cited imaging studies
Functional imaging
Type of imaging
PET Study
Petersen et al. (1989)
Martin et al. (1995)
Grabowski et al. (1996)
Papathanassiou et al. (2000)
fMRI Stoodley and Schmahmann
(2009)
Keren-Happuch et al.
(2014)
Hubrich-Ungureanu et al.
(2002)
SPECT Study
Crossed cerebellar Abe et al. (1997)
diaschisis
Mariën et al. (2001b)
Crossed Mariën et al. (1996)
cerebellocerebral
diaschisis Zettin et al. (1997)
Mariën et al. (2009)
Participants Tasks (control task) Cerebellar activations
17R (11F, 6M) Sensory task (fixation point) None
Output task (passive words) Superior anterior CB (L + R)
Association task (repeat words) Inferior lateral CB (R)/posterior CB (L + R)
12R (3F, 9M) Color word generation (reading aloud) None
Verb generation (reading aloud) Lateral CB (R)
18R Output task (passive words) Inferior lateral CB (R+ L)
Association task (repeat words)
8R (M) Passive story listening (rest) Posterior CB (R > L)
Covert verb generation (rest) Anterior CB (R + L)/posterior CB (R)
Meta-analysis of 11 articles Several different language tasks Lobule VI – crus I (R)/crus I–II – lobule VIIAt
(ALE method) (R)/lobule VI (L)
Meta-analysis of 15 studies Expressive language tasks Lobule VI – midlobule VIII – crus I (R)/crus
(ALE method) Receptive language tasks I (R + L)/crus II (R + L)
crus I (R)/lobule VI (L)
1R (F), 1L (F) Covert phonological verbal fluency (rest) R: CB (R)
L: CB (L)
Patients Deficit(s) Lesion site Hypoperfusion
15 (6F, 9M) Broca’s aphasia Spared base of frontal gyrus None
Base of frontal gyrus CB R< L
83 years R M AoS L anterior insula/adjacent frontal CB R< L
Phonologic agraphia opercular cortex
73 years R M Luria’s dynamic aphasia R SCA Parieto-occipital region (R + L)/
frontoparietal region (L)
46 years R M Expressive agrammatism R CB hematoma Frontotemporal cortex (L)/basal
ganglia (L)/thalamus (L)
58 years R M Mild transcortical sensory R SCA ischemic infarction Medial frontal lobe (L)
aphasia/visual dyslexia/
surface dysgraphia
Continued
Table 11.1
Continued

SPECT Study Patients Deficit(s) Lesion site Hypoperfusion

Baillieux et al. (2010)
De Smet et al. (2011)
18R (6F, 12M) Attention (72%) R CB (vascular: 3 PICA, 3 SCA; Frontal (8/13)
Executive (50%) tumor: 2) Parietal (2/13)
Memory (50%) L CB (vascular: 4 PICA, 1 SCA;
Behavioral/affective (50%) tumor: 1)
Bilateral CB (vascular: 1 SCA)
Vermis (3)
74 years R M Ataxic dysarthria/dynamic R CB hemorrhage Posterior parietal (L)
aphasia/anomia/apraxic Motor/premotor areas (L)
agraphia
86 years R F Ataxic dysarthria/apraxic R > L CB ischemic lesions Parietal lobe (R)
agraphia/mild attention Old R temporoparietal ischemic Motor/premotor areas (R)
problems infarction
76 years R M Apraxic agraphia/frontal R PICA infarction Lateral prefrontal lobe (L + R)
problem solving/mental Old R posterior parietal ischemic Inferior lateral frontal lobe (L + R)
flexibility infarction Inferior medial frontal lobe (L + R)

fMRI, functional magnetic resonance imaging; PET, positron emission tomography; SPECT, single-photon emission computed tomography.
Patients: F, female; L, left-handed; M, male; R, right-handed.
Other columns: ALE, activation likelihood estimation; AoS, apraxia of speech; CB, cerebellum; L, left; PICA, posterior inferior cerebellar artery; R, right; SCA, superior cerebellar artery.
 LANGUAGE AND THE CEREBELLUM
SINGLE-PHOTON EMISSION COMPUTED
TOMOGRAPHY (SPECT)
Crossed (cerebro)cerebellar diaschisis
Evidence for a pattern of crossed activations has also
been provided by a number of SPECT perfusion studies
measuring cerebral blood. Baron et al. (1980) described
the phenomenon of crossed cerebellar diaschisis, denot-
ing the distant functional impact of a supratentorial lesion
on the contralateral cerebellar hemisphere. Crossed cer-
ebellar diaschisis associated with language deficits was
investigated by Abe et al. (1997). They performed a
group study with MRI and SPECT in 30 patients with
chronic Broca’s aphasia after cerebral damage. It was
shown that infarcts affecting the lower part of the left
frontal gyrus of the language-dominant hemisphere were
associated with crossed cerebellar diaschisis, implying
functional and/or anatomic connections of this supraten-
torial region with the right cerebellar hemisphere. Interest-
ingly, patients with crossed cerebellar diaschisis presented
with classic Broca’s aphasia, while patients without dam-
age to the lower left frontal gyrus mainly presented with
word-finding difficulties without additional, more com-
plex language impairments (Abe et al., 1997).
In addition, several case studies using SPECT imaging
in patients with apraxia of speech (AoS) after left insular
infarctions provided support for a close interconnection
between the language-dominant left frontal regions and
the right cerebellum (Mariën et al., 2001b). After an iso-
lated infarction in the precentral gyrus of the language-
dominant insula, directly anterior to the central insular
sulcus, an 83-year-old right-handed patient presented with
severe AoS and phonologic agraphia. A Tc-99m-ethyl
cysteinate dimer (ECD) SPECT scan 9 days after admis-
sion revealed a hypoperfusion in the left inferior frontal
gyrus and precentral gyrus, and in the right cerebellar
hemisphere (Mariën et al., 2001b).
Crossed cerebellocerebral diaschisis
The reversed phenomenon in which (focal) cerebellar
damage exerts a distant functional effect at the supratentor-
ial level is called crossed cerebellocerebral diaschisis.
Decreased cerebral blood flow in the cerebral hemisphere
contralateral to the injured cerebellar hemisphere is an indi-
rect measure of function often found in the anatomoclini-
cally suspected supratentorial regions subserving linguistic
and cognitive functions (Mariën et al., 1996, 2007; Zettin
et al., 1997; Baillieux et al., 2010; De Smet et al., 2011).
Clinical evidence in children
Several different neurodevelopmental disorders associ-
ated with cerebellar involvement may show motor and
187
nonmotor language deficits. The main clinical pictures
are reported below.
CONGENITAL CEREBELLAR MALFORMATIONS
Cerebellar malformations may affect speech and language
development, with a wide spread of severity, ranging from
absence of language to high-level metalinguistic disorders
according to the localization and extent of the defects.
Malformations localized to one or both cerebellar hemi-
spheres and to the vermis may result in permanent recep-
tive and expressive language deficits or may show a slow
and progressive improvement over the following years.
In the case of near total absence of the cerebellum, a very
rare condition in which only a minimal portion of cerebel-
lum is observed, the few patients described (Stewart, 1956;
Romaniello and Borgatti, 2013; Yu et al., 2015) showed
a marked language delay, absent for many years and fol-
lowed by partial acquisition of language skills. In the
patient described by Arrigoni et al. (2015) the language
was less compromised than the motor and relational
abilities: he said two clear words at 24 months, he used
nine clear words at 5 years, he used two words or longer
sentences at 6 years, he used two personal pronouns at
8 years, and learned to read and write at 10 years. The neu-
roimaging study showed a very small component of
cerebellar tissue located posterior to the midbrain, close
to the quadrigeminal plate. Analysis of diffusion tensor
imaging and resting-state fMRI data showed an impair-
ment of the executive-control network, involving areas
strongly connected with the cerebellum through the fron-
topontine fibers.
Despite the improvement over time of deficits asso-
ciated with congenital cerebellar malformations, the
observed clinical picture is often severe and involves
all abilities (motor, cognitive, affective/relational, and lin-
guistic), so it is possible to use the term “congenital” cer-
ebellar cognitive affective syndrome (CCAS) (Tavano
et al., 2007a), referring to the framework described by
Schmahmann and Sherman (1998) in adults affected
by acquired cerebellar lesions (for details on CCAS or
Schmahmann syndrome (Manto and Mariën, 2015) see
section on clinical evidence in adults, below).
The CCAS observable in patients with congenital
malformations seems to be more severe and less specific
than that observed in patients with acquired cerebellar
lesions. However, in patients with cerebellar malforma-
tions, it is more difficult to establish strict anatomic and
functional correlations. However, some general princi-
ples seem to apply: in total or near total vermian cerebel-
lar agenesis the language is completely absent or limited
to single-word utterances (Tavano et al., 2007a). Chil-
dren with vermian hypoplasia may suffer from social
and affective disturbances which are associated with
188 P. MARIËN AND R. BORGATTI
language difficulties. In such cases, both domains tend to
display a similar degree of impairment, which varies
from severe to very mild. Language deficits may be
present at an early age, even in the absence of social
and affective disorders. Malformations confined to the
cerebellar hemispheres display an inverse pattern of
results, sparing social and affective skills and impacting
more severely on the acquisition of cognitive and lan-
guage abilities. In the two cases described by Tavano
et al. (2007b) the expressive abilities were within normal
ranges and the two patients failed only on the grammatic
comprehension test. They presented with diffuse malfor-
mation of cortical development of the cerebellar hemi-
spheres, more extensive on the right side, providing
evidence for a major role of this structure, not only in
language but also specifically in the acquisition of
morphosyntax, possibly subserving procedural memory
systems.
However, in patients with hemispheric cerebellar mal-
formations, it is more difficult to establish strict anatomic
and functional correlations. The early onset of the mal-
formation and the ensuing neural reorganization make
it difficult to establish a neurofunctional profile compa-
rable to that of patients who sustained a lesion later
during life. For example, in a patient presenting with a
complete agenesis of the right cerebellar hemisphere
(Tavano et al., 2007a), language performance was sur-
prisingly in the normal range. This patient presented with
nonfamiliar left manual preference (probably owing to
compensation mechanisms) and a relevant visuospatial
deficit, similar to that of patients sustaining early left-
brain hemisphere lesions.
In nonsyndromic rhombencephalosynapsis, a rare, spo-
radic cerebellar malformation characterized by agenesis of
the vermis, dorsal fusion of the cerebellar hemispheres,
and fusion of DN and superior cerebellar peduncles,
the clinical presentation is variable (Poretti et al., 2009).
Usually cognitive functions are impaired and language
compromised, but subjects with mild intellectual impair-
ment and normal linguistic profile have been occasionally
observed (Toelle et al., 2002; Chemli et al., 2007).
Motor and nonmotor language deficits can be observed
in Joubert syndrome (JS), a rare group of genetically
heterogeneous conditions (ciliopathies) characterized by
a complex malformation of the midbrain–hindbrain con-
sisting of moderate to severe vermian hypo/dysplasia,
associated with thickened, elongated, horizontal superior
cerebellar peduncles resembling a molar tooth on axial
MR images, a neuroradiologic hallmark of the syndrome.
Structural neuroimaging of the cerebellum also shows
hypodysplasia of the cerebellar vermis. Djffusion tensor
imaging reveals a lack of the decussation of the superior
cerebellar peduncles, matching the underlying pathophys-
iology of a ciliopathy.
Clinically JS is characterized by neonatal hypotonia,
psychomotor delay, ataxia, and oculomotor apraxia
(Valente et al., 2008; Romani et al., 2013; Poretti et al.,
2017). Language-related motor deficits consist of oral-
motor dyspraxia, characterized by impaired tongue
movements (lateralization, elevation, and depression).
This defect shares similarities with the deficit in ocular
lateralization movements, responsible for oculomotor
apraxia, typical of JS.
Braddock et al. (2006) described the characteristic
motor speech impairment in JS by submitting 21 patients
to a specific speech and motor language assessment. The
authors found that nearly all participants were able to
protrude their lips as in a pucker, retract their lips as in
a smile, and stick out their tongue past their lips. In con-
trast, only about one-third to one-half of the participants
were able to move their tongue side to side, upward, and
downward. The most notable deficits were in the produc-
tion of alternating movements of the lip, tongue, and
velum. It has been hypothesized that oral-motor dyspraxia
may be due to an abnormal corticobulbar connectivity
related to hindbrain malformations (Braddock et al.,
2006; Arrigoni et al., 2017) and, as the oculomotor
apraxia, it may be related to an impairment of mechanisms
of axonal guidance (Engle, 2010; Lee and Gleeson, 2010).
Nonmotor language deficits in JS are quite similar to
those ascribed generally to cerebellar malformation,
even if some specific differences are present. Tavano
and Borgatti (2010) compared two groups (JS versus
cerebellar-malformed patients). In agreement with the
literature, they found that JS children were significantly
more impaired in expressive language and verbal working
memory with preserved comprehension skills (Steinlin
et al., 1997; Fennell et al., 1999; Braddock et al., 2006).
In a recent study on 76 JS patients, Summers et al.
(2017) confirmed that comprehension was less affected
than expressive language, and that JS children may com-
prehend what others say to them, even if they are not able
to reciprocate that communication. It should be pointed
out that about two-thirds of individuals with JS have some
degree of intellectual disability (Summers et al., 2017).
Abnormal electroencephalogram is noted in association
with lower neuropsychologic functions.
CEREBELLAR INJURIES IN PRETERM INFANTS
During the third trimester of pregnancy the cerebellum
undergoes rapid growth and any potential insult can dis-
rupt the highly complex programmed development of the
cerebellum. Consequently, extremely preterm infants are
particularly susceptible to early injury and subsequent
maldevelopment of the cerebellum (Brossard-Racine
et al., 2015) and it has been estimated that up to 19%
of premature infants born before 32 gestational weeks
 LANGUAGE AND THE CEREBELLUM
have a cerebellar injury, as evidenced by MRI, with
higher rates among extremely low-birth-weight (< 750
grams) infants (Limperopolulos et al., 2005; Steggerda
et al., 2009). Disturbances in cerebellar development
of premature infants are thought to occur both by direct
or indirect cerebellar injury. The first is due to hemor-
rhagic lesions, the latter reflects crossed cerebellar dia-
schisis secondary to a cerebral parenchymal lesion.
Furthermore, cerebellar underdevelopment has also
been described in surviving preterm infants in the absence
of direct cerebellar or cerebral injury, suggesting that
prematurity itself is associated with impaired cerebellar
development (Limperopoulos et al., 2005; Reeber et al.,
2013). Language deficits, both in verbal expressive
abilities as well as in comprehension tasks, are well
documented in preschool and school-aged children born
preterm when a direct or indirect injury is evident on MRI
(Johnsen et al., 2005; Limperopoulos et al., 2007). In
these cases the more severe clinical pictures are associ-
ated with injury involving the vermis. To note, the
lateralized right cerebellar hemispheric language path-
way, clearly reported in adults, is not always evident in
these patients, suggesting the existence of a neural reor-
ganization. More controversial is the role played by the
cerebellum in language deficits and learning disabilities,
which is often observed in premature infants without a
documented/matching lesion on MRI (Brossard-Racine
et al., 2015).
POSTERIOR FOSSA SYNDROME
The posterior fossa syndrome, described by Daly and
Love in 1958, is the first demonstration in children of
cerebellum involvement in language deficits. It consists
of language, behavioral, and affective disturbances asso-
ciated with executive dysfunction after posterior fossa
surgery. Language difficulties include cerebellar mutism
as well as anomia, difficulties with semantic and prag-
matic language, and agrammatism (Salman and Tsai,
2016). After this first description, several studies have
reported a variety of language deficits following acquired
cerebellar damage in children affected by tumors
(Copeland et al., 1999; Levisohn et al., 2000; Riva and
Giorgi, 2000; Docking et al., 2007; De Witte et al.,
2017) or after vascular stroke (Karaci et al., 2008;
Mariën et al., 2009; van Dun et al., 2015).
As in adulthood, when a relationship between loca-
tion of damage and outcome is established (see section
on clinical evidence in adults, below), also in children
right posterolateral cerebellar damage is associated with
deficits, including expressive semantic and syntactic lan-
guage, receptive language, and word finding. Levisohn
et al. (2000) studied 19 children treated surgically for cer-
ebellar tumors and demonstrated deficits in executive
189
functions, visuospatial abilities, expressive language
abilities, and verbal memory as well as in the communi-
cative modulation of emotions.
Similar findings were provided by Riva and Giorgi
(2000), who studied 26 children who underwent surgical
treatment for cerebellar hemisphere or vermian tumors.
Vermian lesions, resulting from the excision of medullo-
blastomas, were associated with two different outcomes:
(1) postsurgical mutism, which evolved into speech or
language disorders; or (2) disturbances of social and
communication behavior, ranging from irritability to
autistic symptoms, with lesions involving the posteroin-
ferior lobules of the vermis. Children with a right cerebel-
lar hemispheric tumor (astrocytoma) showed a decline in
verbal abilities, which was, however, nonsignificant,
together with a marked impairment in complex aspects
of language, such as the mean length of utterance. Chil-
dren with left cerebellar tumors also showed a decline in
nonverbal abilities together with a more marked decrease
in executive functions. However, they also presented
with a marked impairment in lexical access both on tap-
ping comprehension and expressive skills.
LEARNING DISABILITIES
As outlined above, cerebellar dysfunctions in children are
often associated with deficits in several neuropsychologic
domains (spatial cognition, visuospatial organization,
attention, planning, set shifting, abstract reasoning, verbal
fluency, and working memory, and so on), all domains
closely related to the learning mechanisms of reading,
writing, and computing. Therefore it is not uncommon
to observe learning disabilities in children with cerebellar
disorders. In addition, the association with cerebellar
abnormalities is largely postulated in a specific learning
impairment named developmental dyslexia (Nicolson
et al., 2001). According to the Diagnostic and Statistic
Manual of Mental Disorders, fifth edition (DSM-5)
(American Psychiatric Association, 2013), developmental
dyslexia refers to a pattern of learning difficulties charac-
terized by problems with accurate or fluent word recogni-
tion, poor decoding, and poor spelling abilities despite
conventional instruction, adequate intelligence, and socio-
cultural opportunity. During the last decades many hypoth-
eses aimed to explain dyslexia but nowadays it is fairly
well accepted that dyslexia is not a unique entity,
although it may reflect different underlying neurocogni-
tive pathologies (Pernet et al., 2009). Among them, the
cerebellar deficit hypothesis relates dyslexia to a general
learning disorder that includes failure to automatize dif-
ferent language-based processes such as grapheme/
phoneme correspondence and/or rapid access to lexicon
entries (Nicolson and Fawcett, 2011; Norton et al., 2014;
Stoodley and Limperopoulos, 2016).
190 P. MARIËN AND R. BORGATTI
Stoodley and Stein (2013) suggested that the cerebel-
lar regions involved in developmental dyslexia tend to be
those that are engaged in language and working-memory
paradigms, even though the results obtained through
functional MR investigations differ in children and
adults. Pernet et al. (2009) found in a sample of 38 dys-
lexic adults structural abnormalities in lobule VI of the
right cerebellum, but cerebellar differences were not
observed in pre-reading children at risk for dyslexia
(Bishop, 2002; Raschle et al., 2011), suggesting that dif-
ferences in the cerebellum may be the consequence of
reading difficulties rather than pre-existing and causal.
Clinical evidence in adults
Clinically, several different types of motor and nonmotor
language deficits have been reported after cerebellar
damage, ranging from pure motor speech disorders to
high-level metalinguistic disturbances (Table 11.2).
MOTOR SPEECH PRODUCTION
Ataxic dysarthria (Holmes, 1917) is a typical cerebellar
motor speech disorder, mainly characterized by distorted
articulation and prosody (Spencer and Slocomb, 2007).
Traditionally, ataxic dysarthria is considered a disorder
of motor execution. However, recent studies have mod-
ified this view to also include disruption of motor speech
programming in addition to a dysfunctional execution
of speech (Mariën and Verhoeven, 2007; Spencer and
Slocomb, 2007). This was based on some typical charac-
teristics of ataxic dysarthria which are more compatible
with a programming/planning disorder than with an
execution one (Spencer and Slocomb, 2007). Moreover,
ataxic dysarthria seems to share some overt semiologic
characteristics with AoS, which has led to the hypothesis
that both disorders are subserved by related pathophysi-
ologic mechanisms (Mariën et al., 2006). Mariën et al.
(2006) and Mariën and Verhoeven (2007) observed a
significant correlation between the perfusional deficits
in the right cerebellum and the remission of AoS symp-
toms in 2 patients with a subtype of AoS, suggesting
an involvement of the cerebellum in the planning and
programming of motor speech.
VERBAL FLUENCY AND LANGUAGE DYNAMICS
In patients with focal and degenerative cerebellar lesions
disruption of verbal fluency and language dynamics has
repeatedly been observed (Leggio et al., 2000; Peterburs
et al., 2010; Schweizer et al., 2010). Typically phono-
logic fluency is more prominently affected than semantic
fluency. Although Hubrich-Ungureanu et al. (2002)
confirmed lateralization of cerebellar involvement in a
(silent) phonologic fluency task and Schweizer et al.
(2010) observed a clear lateralization effect, a number
of other studies contradict unilateral involvement of
the cerebellum in verbal fluency tasks (Leggio et al.,
2000; Cook et al., 2004). However, despite conflicting
results with respect to laterality, a consensus exists with
regard to the role for the cerebellum in verbal fluency and
lexical retrieval (Mariën et al., 2014).
Mariën et al. (1996) described a patient who, after
an ischemic infarction in the vascular territory of the
right superior cerebellar artery, presented with aphasic
symptoms corresponding to Luria’s dynamic aphasia
(characterized by severely reduced, adynamic, fragmen-
ted self-generated speech despite normal confrontational
naming and phonologic skills). A review by Mariën et al.
(2001a) disclosed several additional cases in which
language dynamics were consistently disturbed after
(right) cerebellar damage, resembling transcortical motor
aphasia (Riva, 1998; Gasparini et al., 1999; Fabbro et al.,
2000). Disruption of language dynamics also character-
izes the posterior fossa syndrome.
GRAMMATIC/SYNTACTIC PROCESSING
Grammatic and syntactic disorders are also associated
with cerebellar damage. Both expressive (Silveri et al.,
1994; Zettin et al., 1997) and receptive agrammatism
(Ackermann et al., 1999) have been observed. In most
cases, the grammatic disorders are caused by right cerebel-
lar lesions (Silveri et al., 1994; Mariën et al., 1996, 2000;
Zettin et al., 1997; Gasparini et al., 1999). However, there
are a few reports of patients with left cerebellar lesions
who also presented with grammatic and/or syntactic def-
icits (Justus, 2004; Adamaszek et al., 2012).
READING
Only a handful of cases have been described in which
acquired cerebellar damage leads to reading difficulties
(Moretti et al., 2002; Mariën et al., 2009). Moretti et al.
(2002) demonstrated that patients with cerebellar lesions
made more errors at letter and word level in reading words
and sentences compared to right-handed controls. More
recently, Mariën et al. (2009) reported a patient with visual
dyslexia after an ischemic infarction in the vascular terri-
tory of the right superior cerebellar artery. A quantified
SPECT study showed a relative hypoperfusion of the right
cerebellar hemisphere and the left medial frontal lobe,
which may be caused by functional disruption of the cer-
ebellocerebral pathways (Mariën et al., 2009).
WRITING
In the last few decades, cerebellar lesions have been
frequently associated with writing disorders. Different
types of peripheral agraphias (allographic agraphia,
apraxic agraphia, motor execution agraphia (micrographia
and megalographia), hemianoptic agraphia, and afferent
Table 11.2
Overview of cited case reports

Clinical evidence

Language
deficit Study Patient Deficits Lesion site Imaging

Motor speech Mariën and 53 years R F FAS Frontoparietal stroke SPECT (33 days poststroke):
production Verhoeven (2007) hypoperfusion in CB (R)
61 years R M Conduction-like aphasia/FAS L basal ganglia SPECT (1 month poststroke):
hemorrhage into hypoperfusion in CB (R)
L parietotemporal
region
Spencer and 20 studies (healthy participants) None None fMRI/PET/ERP
Slocomb (2007) 19 studies (dysarthric patients) Ataxic dysarthria Cerebellar lesions fMRI/PET
Bilateral superior CB: speech
motor control
R CB: planning and
processing of speech
Verbal fluency Leggio et al. (2000) 25 patients (cerebellar disease) Phonemic fluency: CB patients < controls Focal or degenerative
14 healthy controls Semantic fluency: CB patients
controls CB disease
(L: n ¼ 13; R: n ¼ 6;
idiopathic: n ¼ 6)
Schweizer et al. 22 patients (chronic cerebellar Phonemic fluency: R CB patients < L CB L CB: n ¼ 12
(2010) lesions) patients
controls R CB: n ¼ 10
30 healthy controls Semantic fluency: R CB patients <
controls
Cook et al. (2004) 5 patients (vascular cerebellar Phonemic fluency/sentence L CB (ischemic or
lesions) construction/word definitions/multiple hemorrhagic)
definitions/figurative language/word
associations/semantic absurdities/
synonyms/ antonyms
Mariën et al. (1996) 73 years R M Luria’s dynamic aphasia R SCA SPECT (30 days poststroke):
hypoperfusion in
parieto-occipital region
(R + L)
frontoparietal region (L)
Riva (1998) 4 years 2 months F Mutism -> reduced spontaneous speech/ Viral cerebellitis
aphonic/aprosodic/sequential memory
Gasparini et al. 51 years R M Agrammatism/dysprosody R CB infarction SPECT: hypoperfusion in
(1999) R CB

Continued
Table 11.2
Continued

Clinical evidence

Language
deficit Study Patient Deficits Lesion site Imaging

Fabbro et al. (2000) 21 years R M Syntax/synonyms/attribute generation Arachnoidal cyst in PF

28 years R F Synonym/arithmetics/writing to dictation Hemangioblastoma
in PF
48 years R M Dysarthria/fluency/propositioning/lexical CB astrocytoma in
access/morphology/syntax/semantics/ vermis
behavioral/writing to dictation
59 years F Grammar/arithmetics/ reading/syntax/ L CB astrocytoma
writing to dictation
Riva and Giorgi 26 patients Mutism ! dysarthria R CB astrocytoma
(2000) or (n ¼ 7)
Affective/social behavioral disturbances L CB astrocytoma
(n ¼ 8)
CB vermis
medulloblastoma
(n ¼ 11)
Grammatical/ Silveri et al. (1994) 67 years R M Expressive agrammatism R CB infarct SPECT (5 weeks poststroke):
syntactical hypoperfusion in:
processing cerebral hemisphere (L)
Zettin et al. (1997) 46 years R M Expressive agrammatism R CB hematoma SPECT (4 weeks poststroke):
hypoperfusion in
frontotemporal cortex (L)
Basal ganglia (L)
Thalamus (L)
Ackermann et al. 9 (3F, 6M) Ataxia/receptive agrammatism Degenerative cerebellar
(1999) atrophy
Mariën et al. (1996) 73 years R M Luria’s dynamic aphasia R SCA SPECT (30 days poststroke):
hypoperfusion in
parieto-occipital region
(R + L)
Frontoparietal region (L)
Gasparini et al. 51 years R M Agrammatism/dysprosody R CB infarction SPECT: hypoperfusion in
(1999) R CB
Table 11.2
Continued

Clinical evidence

Language
deficit Study Patient Deficits Lesion site Imaging

Justus (2004) 16 patients Grammatical morphology R CB (n ¼ 3)

16 controls L CB (n ¼ 3)
Midline CB (n ¼ 1)
Bilateral CB (n ¼ 9)
Adamaszek et al. 8R patients (1F, 7M) Syntactic processing R CB (n ¼ 2)
(2012) 8R controls (2F, 6M) L CB (n ¼ 6)
Reading Moretti et al. (2002) 10R patients (4F, 6M) Reading Vermian/paravermian
10R controls (5F, 5M) tumor
Mariën et al. (2009) 58 years R M Mild transcortical sensory aphasia/visual R SCA ischemic SPECT (5 weeks poststroke):
dyslexia/surface dysgraphia infarction hypoperfusion in
CB (R)
Medial frontal lobe (L)
Writing Silveri et al. (1997) 67 years R M Spatial dysgraphia Cerebellar atrophy
Silveri et al. (1999) 26 years R F Spatial dysgraphia CB hemorrhage (vermis
+ R > L hemisphere)
Mariën et al. (2007) 72 years R M Apraxic agraphia R CB hemorrhage SPECT (1 and 6 months
poststroke):
hypoperfusion in
CB (R)
Medial/lateral prefrontal
area (L)
De Smet et al. (2011) 74 years R M Ataxic dysarthria/dynamic aphasia/ R CB haemorrhage SPECT (1 and 6 months
anomia/apraxic agraphia poststroke):
hypoperfusion in
posterior parietal (L)
Motor/premotor areas (L)
86 years R F Ataxic dysarthria/apraxic agraphia/mild R > L CB ischemic SPECT (1 and 6 months
attention problems lesions poststroke):
Old R temporoparietal hypoperfusion in
ischemic infarction parietal lobe (R)
Motor/premotor areas (R)

Continued
Table 11.2
Continued

Clinical evidence

Language
deficit Study Patient Deficits Lesion site Imaging

76 years R M Apraxic agraphia/frontal problem solving/ R PICA infarction SPECT (2 weeks poststroke):
mental flexibility Old R posterior parietal hypoperfusion in
ischemic infarction lateral prefrontal lobe (L + R)
Inferior lateral frontal lobe
(L + R)
Inferior medial frontal lobe
(L + R)
Mariën et al. (2009) 58 years R M Mild transcortical sensory aphasia/visual R SCA ischemic SPECT (5 weeks poststroke):
dyslexia/surface dysgraphia infarction hypoperfusion in
CB (R)
Medial frontal lobe (L)
Fabbro et al. (2000) 28 years R F Synonym/arithmetics/writing to dictation Hemangioblastoma
in PF
48 years R M Dysarthria/fluency/ propositioning/lexical CB astrocytoma in
access/morphology/syntax/ semantics/ vermis
behavioral/writing to dictation
59 years F Grammar/arithmetics/ reading/syntax/ L CB astrocytoma
writing to dictation
Fabbro (2004) 26 years R M Writing to dictation L CB ischemic
infarction
30 years R M Writing to dictation L CB ischemic
infarction
van Gaalen et al. 29 patients Writing to dictation SCA 6
(2014)
Metalinguistic Cook et al. (2004) 5 patients (vascular cerebellar Phonemic fluency/sentence L CB (ischemic or
skills lesions) construction/word definitions/multiple hemorrhagic)
definitions/figurative language/word
associations/semantic absurdities/
synonyms/ antonyms
Whelan and 2 patients Recreating sentences/antonyms/ L CB vascular infarct
Murdoch (2005) 16 healthy controls definition/multiple definitions
Murdoch and 10R patients (2F, 8M) Phonemic fluency/sentence formulation/ L CB (ischemic or
Whelan (2007) 10R controls lexical-semantic manipulation hemorrhagic)

Patients: F, female; L, left-handed; M, male; R, right-handed.

Other columns: CB, cerebellum; ERP, evoked related potential; FAS, foreign accent syndrome; fMRI, functional magnetic resonance imaging; L, left; PET, positron emission tomography; PF, posterior fossa;
PICA, posterior inferior cerebellar artery; R, right; SCA, superior cerebellar artery; SCA 6, spinocerebellar ataxia 6; SPECT, single-photon emission computed tomography.
 LANGUAGE AND THE CEREBELLUM
or neglect dysgraphia), a group of disorders of the coordi-
nation, planning, and execution of writing movements,
not attributable to motor or sensory impairments and the
central agraphias, involving the central spelling processes
lexical (or surface) agraphia, phonologic agraphia, deep
agraphia, semantic agraphia and agraphia due to impair-
ment of the graphemic buffer, have been reported.
Silveri et al. (1997, 1999) described 2 patients with
spatial dysgraphia after cerebellar damage. The same
type of written language impairment was reported by
Fournier del Castillo et al. (2010) in a pediatric patient.
They described an 8-year-old patient who developed
apraxic agraphia in a context of cerebellar atrophy sec-
ondary to acute cerebellar swelling at the age of 4.6 years.
Frings et al. (2010) identified megalographia in 6 chil-
dren with chronic surgical cerebellar lesions following
posterior fossa tumor resection.
Several patients have been reported with acquired
apraxic agraphia following focal cerebellar damage
(Mariën et al., 2007; De Smet et al., 2011) or in the con-
text of a neurodevelopmental disorder (Mariën et al.,
2013). Quantified ECD SPECT studies in patients with
apraxic agraphia consistently showed reduced perfusion
in the medial prefrontal regions of the left hemisphere,
known to be involved in the planning and execution of
skilled graphomotor actions, and the right cerebellum.
The central agraphias on the other hand are only
scarcely reported after cerebellar damage. Mariën et al.
(2009) described a patient with surface dysgraphia
(together with visual dyslexia) after an ischemic infarction
in the vascular territory of the right superior cerebellar
artery. A quantified SPECTstudy showed a hypoperfusion
of the left medial frontal lobe. Other possible cases of
central agraphia are difficult to evaluate due to limited
information about the observed writing disorder (Fabbro
et al., 2000; Fabbro, 2004; van Gaalen et al., 2014).
METALINGUISTIC SKILLS
Several studies point to an involvement of the left cerebel-
lar hemisphere in higher-level language and metalinguistic
skills. Some patients with primary left cerebellar stroke are
known to have difficulties with providing multiple defini-
tions for homophonic words, recreating sentences, figura-
tive and ambiguous language, word associations, antonym/
synonym generation, and interpreting semantic absurdities
(Cook et al., 2004; Whelan and Murdoch, 2005; Murdoch
and Whelan, 2007; Guell et al., 2015). Disruption of meta-
linguistic skills is typically associated with right cerebral
damage (Kempler et al., 1999). From an anatomoclinical
point of view this indicates that metalinguistic processes
are more dependent on the left cerebellum–right hemi-
sphere network than traditional language skills.
195
POSSIBLE PATHOPHYSIOLOGIC
MECHANISMS AND COGNITIVE
THEORIES FOR CEREBELLAR
INVOLVEMENT IN LANGUAGE
Several different hypotheses have been put forward to
explain the pathophysiologic and cognitive mechanisms
by means of which the cerebellum plays a role in linguis-
tic processes.
Pathophysiologic mechanisms
In 1987 Broich et al. for the first time described crossed
cerebellocerebral diaschisis after a cerebellar infarction.
Their SPECT study showed a relative hypoperfusion of
the contralateral left hemisphere in a patient with a right
cerebellar infarction. The authors hypothesized that
crossed perfusional deficits reflect a functional depres-
sion of the supratentorial areas due to a lack of excitatory
stimuli through the cerebellothalamocerebral pathways
which connect the cerebellum to several cerebral associ-
ation areas crucially implicated in cognitive and affective
processing.
Since then, crossed cerebellocerebral diaschisis has
been frequently reported in patients with speech and
language deficits after cerebellar damage (Hassid,
1995; Mariën et al., 1996, 2000, 2007; Zettin et al.,
1997; Baillieux et al., 2010; De Smet et al., 2011). For
example, Mariën et al. (1996) described a 73-year-old
right-handed man with an ischemic infarction in the right
superior cerebellum. The patient presented with aphasic
symptoms closely resembling Luria’s dynamic aphasia,
complicated by receptive and expressive agrammatism.
SPECT findings revealed relative hypoperfusions in
the anatomoclinically suspected prefrontal regions of the
language-dominant hemisphere. Moreover, the pattern
of perfusional deficits mirrored linguistic recovery: the
prefrontal language regions regained normal perfusion
when remission of the aphasic symptoms was observed.
This evidence strongly suggests a link between crossed
cerebellocerebral diaschisis and cerebellar-induced lan-
guage disturbances (Mariën et al., 1996, 2000).
Cognitive theories
In 1998, Schmahmann and Sherman introduced the con-
cept of CCAS or Schmahmann syndrome (Manto and
Mariën, 2015). After screening and testing 20 patients
with isolated cerebellar lesions, they identified a cluster
of symptoms that could be classified into four categories:
(1) executive dysfunctions (planning, set shifting, abstract
reasoning, and working memory); (2) visuospatial deficits
(visuospatial organization and memory); (3) behavioral-
affective disturbances (blunting of affect or disinhibited
and inappropriate behavior); and (4) language symptoms
196 P. MARIËN AND R. BORGATTI
CEREBELLUM
UNIVERSAL CEREBELLAR TRANSFORM
MOVEMENT NEUROCOGNITION AFFECT
Fig. 11.3. Schematic representation of the dysmetria of thought theory. (Adapted from Guell et al. (2015) with permission from
Springer.)
(agrammatism and anomia) (Schmahmann and Sherman,
1998). To explain the cerebellar-induced deficits,
Schmahmann (1998) proposed the “dysmetria of thought
theory,” which draws analogies with the motor system
(dysmetria of movement) (Fig. 11.3). This hypothesis sug-
gests a role for the cerebellum as a modulator of cognitive
and affective function that compares the intended outcome
with the perceived outcome to detect and prevent or cor-
rect mismatches. Schmahmann (1998) hypothesized that
the cerebellum acts as an oscillation dampener, smoothing
out performance of mental operations (Schmahmann,
1998; Mariën et al., 2014).
Due to its architectural homogeneity and its dense
interconnections with the supratentorial association areas,
it is frequently stated that the cerebellum contributes to
both motor and nonmotor activities in a similar manner.
Schmahmann referred to this unique computation as the
“universal cerebellar transform” (Schmahmann, 2000;
Koziol et al., 2014) (Fig. 11.3). This phenomenon allows
the cerebellum to compare predictions related to “internal
models” (¼ “any neural representation of the external
world” (Ito, 2008)) with the incoming feedback from
the cerebrum, thus optimizing human behavior and perfor-
mance. This explanation is in accordance with the concept
of “dysmetria of thought” that Schmahmann introduced
in 1998 and which implies a “universal cerebellar impair-
ment.”. If the cerebellum is involved in every cortical
process in the same way, cerebellar damage should result
in a similar kind of disruption of these processes (Koziol
et al., 2014). Both universal cerebellar transform and
universal cerebellar impairment have a strong anatomic
substrate given the homogeneous morphology of the
cerebellar microcomplexes throughout the cerebellar cir-
cuitry. In this context, Schmahmann reported in a number
of studies that every deficit resulting from cerebellar
damage can be interpreted as hypometric/diminished or
hypermetric/exaggerated behaviors (for an overview, see
Koziol et al., 2014). As a result, the theories relating to
motor dysfunction and cerebellar disease were adapted to
CEREBELLAR DAMAGE
IMPAIRED UNIVERSAL CEREBELLAR TRANSFORM
DYSMETRIA OF DYSMETRIA OF
MOVEMENT THOUGHT
SCHMAHMANN’S
ATAXIA
SYNDROME
account for the observed linguistic deficits after cerebellar
damage (Strick et al., 2009; Mariën et al., 2014).
Internal models have been used to explain the ability
to perform controlled and skillful movements by creating
a prediction of the dynamics of a body part. These pre-
dictions help to perform a complex movement in a very
precise way without constantly relying on sensory feed-
back (Ito, 2008). Ito (2008) hypothesized that these inter-
nal models can be used in the same manner to create and
manipulate mental representations, in association with the
prefrontal and temporoparietal cortex. These models have
also been used to explain the involvement of the cerebel-
lum in language (Mariën et al., 2014). In language studies
the cerebellum is frequently regarded as a predictor of
future states (as in the “dysmetria of thought” hypothesis
(Schmahmann, 1998)) that use these predictions to opti-
mize cognitive and language functioning by comparing
them with the cortical feedback (Mariën et al., 2014).
However, which mechanism the cerebellum applies to
constitute these predictions remains a matter of debate
(Leggio and Molinari, 2015). Below, two main hypotheses
of the motor literature are discussed in the context of cog-
nitive and language functions. These two theories are fre-
quently cited in studies that found involvement of the
cerebellum in language functioning (Mariën et al., 2014).
TIMING HYPOTHESIS
Keele and Ivry (1990) suggested that the cerebellum is
responsible for the temporal computation of a number
of different tasks. This hypothesis was primarily based
on observations of timing deficits in cerebellar patients,
and on the unique anatomic structure of the cerebellum
(for instance, the delay lines corresponding to the Pur-
kinje neurons crossed by given parallel fibers) which
lends itself perfectly to temporal processing (Spencer
and Ivry, 2013). Patients with cerebellar disorders had
trouble judging the velocity of moving visual stimuli
and differentiating between two auditory stimuli of
 LANGUAGE AND THE CEREBELLUM
different lengths. As a result, Keele and Ivry (1990) pro-
posed a role for the cerebellum in providing temporal
information in motor coordination. According to these
authors, the cerebellum is not only responsible for the
timing of the different movements but also incorporates
cortical input to adjust this timing accordingly, such as in
locomotion. The cerebellum is therefore responsible for
the timing of the expected feedback and the actual feed-
back. If an expected feedback comes earlier or later than
expected, it will be treated as an unexpected event due to
the timing coordination of the cerebellum (Gellman et al.,
1985; Keele and Ivry, 1990). Silveri et al. (1994) and
Gasparini et al. (1999), for instance, used the timing
hypothesis to explain the linguistic deficits observed
after right cerebellar damage in their patients. They spec-
ulated that the expressive agrammatism they observed in
patients with cerebellar lesions might be the result of a
delay in the application of syntactic rules and linguistic
processes (Gasparini et al., 1999). Due to this delay, caused
by the damage to the cerebellum, the information held in
the verbal working memory decays before all the opera-
tions are performed, resulting in errors (Silveri et al.,
1994; Gasparini et al., 1999). As such, the cerebellum times
the linguistic operations performed on the information
held in the verbal working memory. Recently, Schwartze
and Kotz (2016) have theorized about the role of the cere-
bellum in speech perception based on a computational
model of temporal processing. They speculated that the
temporal features of speech may be exploited by the cere-
bellum to coordinate the cortical regions involved in lan-
guage comprehension. They considered the cerebellum
to be a modular clock-like system preparing the cortical
regions in a timely manner to optimize speech perception.
SEQUENCING HYPOTHESIS
Another explanation of cerebellar involvement in lan-
guage is provided by the sequencing hypothesis. The cer-
ebellum as a monitor of sequential events has already been
proven in the somatosensory system using expected and
unexpected stimuli (Leggio et al., 2011). With respect to
language, it is hypothesized that the activity of different
functional modules, necessary to perform linguistic pro-
cesses, is synchronized and coordinated by the cerebellum.
The cerebellum would act as a monitor and supervisor of
the sequence in which linguistic processes are performed,
integrating its activity with the so-called “frontal-lobe
system” (Fabbro et al., 2000). Especially in novel strate-
gies (e.g., used in phonologic fluency), the cerebellum
might play an important role in smoothing and speeding
up the process (Leggio et al., 2011; Mariën et al., 2014).
It is also believed that the cerebellum is responsible
for both the temporal and sequential organization of
both overt and covert speech (Ackermann, 2008).
197
Ackermann et al. (2004) suggested that cognitive deficits
observed after cerebellar damage could be due to an
impairment of the “inner speech,” which can compromise
verbal working memory (Koziol et al., 2014). The perfor-
mance on cognitive operations involving a generation of a
pre-articulatory speech code most likely suffers if this
“inner speech” function is compromised (Ackermann
et al., 2004).
A lateralized linguistic cerebellum
All suggested cognitive theories strongly rely on the
crossed functional cerebellocerebral connections, via
which the cerebellum exerts its modulatory influence
on the cognitive functions subserved by the supratentorial
areas. Each of these theories regards the cerebellum as a
coordinator/modulator of supratentorial motor, cognitive,
and affective processes, recognizing the cerebellum as a
nonspecific high-level operational device that provides
active support to a variety of functions in a similar manner
(Mariën et al., 2014). Since in the vast majority of right-
handers ( 97%) and in most left-handers ( 70%)
the left hemisphere is dominant for language (Knecht
et al., 2000; Mariën et al., 2004), it is assumed that the
involvement of the cerebellum in language functions is
strongly lateralized to the right hemisphere, while the
left cerebellar hemisphere primarily contributes to right-
hemisphere functioning (Mariën et al., 2001a; Stoodley
and Schmahmann, 2009).
Several studies have shown that the configuration of
language lateralization at the supratentorial level is
strongly related to a contralateral lateralized language
representation at the cerebellar level. Jansen et al.
(2005) showed that atypical right-hemisphere language
dominance is accompanied by a left-lateralized cerebel-
lar contribution to language. Additionally, Mendez
Orellana et al. (2014) found a significant dependency
between language lateralization in the cerebrum and
the cerebellum with an inverse correlation of cerebro-
cerebellar lateralization. This means that the stronger
the language lateralization in the cerebral hemisphere,
the stronger the contralateral cerebellar hemisphere is
involved in language.
Clinically, this is confirmed by a study of Baillieux
et al. (2010). They systematically investigated 18 patients
with primary cerebellar lesions by means of an extensive
neuropsychologic battery of tests. Although distur-
bances of attention, executive function, and memory
were most commonly found, their analyses supported
the hypothesis of a functionally lateralized linguistic
cerebellum, with the right cerebellum being associated
with logical reasoning and language processing, and
the left cerebellum with attentional and visuospatial
skills (Baillieux et al., 2010).
198 P. MARIËN AND R. BORGATTI
CONCLUSIONS Hypothetically, it might be argued that a timing deficit
leads to errors in which not all linguistic operations are
Converging evidence from an increasing number of neu-
successfully completed, such as the use of infinitives
roanatomic, neurophysiologic, neuroimaging, and clini-
instead of a conjugated verb in agrammatism. Due to
cal studies unambiguously shows that the cerebellum
the delay caused by the timing deficit, as hypothesized
plays a cardinal role in a variety of linguistic processes
by Silveri et al. (1994) and Gasparini et al. (1999), the
via a dense network of crossed cerebellocerebral connec-
information temporarily stored in the working-memory
tions. These crossed connections have led to the concept
system decays before all operations are completed
of a "lateralized linguistic cerebellum" in which the right
(Silveri et al., 1994; Gasparini et al., 1999). However,
cerebellar hemisphere is involved in left-hemispheric,
a timing deficit, as described by Keele and Ivry (1990)
and the left cerebellar hemisphere in right-hemispheric,
and Gellman et al. (1985), could lead to other kinds of
functioning (Mariën et al., 2001a). Many SPECT studies
errors due to a deficit in timing and coordinating the cor-
in patients with cerebellar disorders have demonstrated the
tical feedback. This hypothesis merely predicts a disrup-
functional impact of cerebellar pathology on a remote,
tion of the incorporation of the cortical feedback due to
structurally intact language area, suggesting crossed cere-
an inaccurate timing of the expected and the actual input
bellocerebral diaschisis as the possible pathophysiologic
which might lead to a variety of linguistic errors.
mechanism underlying the observed linguistic deficits in
The sequencing hypothesis (Leggio and Molinari,
both acquired and developmental disorders.
2015), on the other hand, predicts a deficit in the coordi-
Due to the architectural homogeneity of the cerebel-
nation and monitoring of the sequence of application of
lum, a universal cerebellar transform mechanism was
different linguistic operations. According to this hypoth-
proposed by Schmahmann (2000), resulting in a
esis, repetitive patterns of temporally or spatially struc-
“universal cerebellar impairment” at the motor, cogni-
tured serial events are identified and simulated by the
tive, and affective level. According to this hypothesis
cerebellum. On the basis of this the cerebellum generates
the cerebellum acts as a coordinator/modulator of both
internal models that can be used to make predictions.
motor and nonmotor (cognitive/affective) functions by
Disruption of serial pattern detection and prediction,
comparing cortical feedback with “internal models.”
and processing of anticipation might not only lead to
These models are internal representations/predictions
the use of infinitives instead of a conjugated verb, but
of future states (Mariën et al., 2014). Recent physiologic
also to wrongly conjugated verbs.
evidence in animal studies strengthens the hypothesis of
In the literature on the role of the cerebellum in motor
a cerebellar contribution to different cortical functions.
processing, both timing and sequencing deficits have been
The timing-dependent plasticity of cerebellar modules
observed after cerebellar damage (timing: Keele and Ivry,
varies from region to region, and may be tuned to the
1990; sequencing: Leggio et al., 2011). It is therefore pos-
specific needs of different tasks/processes (Suvrathan
sible that the cerebellum is involved in both mechanisms,
et al., 2016; Sokolov et al., 2017).
resulting in complicated linguistic errors due to both tim-
Which mechanism is responsible for making these
ing and sequencing deficits. However, the cerebellum is
“internal models” is still a matter of debate. The
not the only structure that uses prediction and the specific
“dysmetria of thought” theory indicates that the cerebellum
role of the cerebellum in the formation and use of internal
tries to keep motor and cognitive processes around a
models remains unclear. In addition, hypotheses about the
homeostatic baseline, acting like an oscillation dampener,
cerebellar coordination of cognitive processes are difficult
without specifying which aspects of the processes are mon-
to verify, and it is not yet clear which cognitive informa-
itored (Schmahmann, 1998). Two factors adapted from
tion the cerebellum might use to form internal models and
the motor literature have been discussed in this chapter
coordinate these processes.
that may hypothetically account for observed language
In conclusion, it can be stated that the cerebellum
disturbances: timing and sequencing. Both mechanisms
contributes in a unique way to the modulation and coor-
have been dealt with in the literature to explain the
dination of a variety of motor and nonmotor (cognitive/
observed language deficits (timing: Silveri et al., 1994;
affective) processes. Examining the precise nature of this
Gasparini et al., 1999; sequencing: Fabbro et al., 2000;
cerebellar contribution is an exciting and challenging
Ackermann et al., 2004). However, future studies are
new research domain.
needed to unravel the specific involvement of the cerebel-
lum in cognitive functioning, as it is not always clear which
ACKNOWLEDGMENTS
language deficits are due to a timing deficit, which to a
disruption of sequencing, and which are merely due to dis- The authors wish to thank Kim van Dun for her contribu-
turbed attention control. tion to this chapter.
 LANGUAGE AND THE CEREBELLUM
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