FUNCTIONAL VIGNETTE
Nonmotor Functions of the Cerebellum: An Introduction
X A.P. Klein, X J.L. Ulmer, X S.A. Quinet, X V. Mathews, and X L.P. Mark
T
he concept of nonmotor functions of the cerebellum (little
cerebrum)
1
is an intriguing proposal that has garnered little
attention in the past but has become a relatively recent focal point
for neuroscience investigators. The preponderance of anatomic
and clinical evidence supporting the traditional view of the cere-
bellum as a motor mechanism has understandably overwhelmed
the sporadic reports of behavioral and intellectual dysfunction
associated with cerebellar pathology during the 19th and most
of the 20th century.
2-7
Developments during the past 25 years,
coinciding with the development of functional MR imaging,
however, have greatly increased our awareness and under-
standing of cerebellar cognitive functions. Neuroimaging in
conjunction with anatomic and clinical investigations is help-
ing to cultivate new ways of thinking about cerebellar organi-
zation and function. This vignette will introduce some of these
major observations of nonmotor cerebellar functions from a
neuroradiologic perspective.
The correlation of cerebellar function and morphology has
been a long-standing mystery that raises interesting questions.
Although the cerebellum accounts for only about 10% of the mass
of the brain, why does it contain as many neurons as all the rest of
the central nervous system combined?
1
Does this imply the
existence of underappreciated functions beyond modulation of
motor activities? Why did the lateral aspect of the human cerebel-
lum, the cerebellar hemispheres, undergo enormous enlargement
during the course of human evolution?
8
Furthermore, why did
this lateral cerebellar growth seem to parallel the evolutionary
enlargement of the prefrontal cortex?
9,10
Functional MR imaging
combined with clinical observations provide a novel backdrop to
frame the answers.
More recent concepts of cerebellar organization provide a
more complete picture of the cerebellum. The traditional mor-
phologic description of the cerebellum subdivides it into lobes,
lobules, and zones (
Fig 1). The phylogenetic description cate-
gorizes the cerebellum into the vestibulocerebellum (archicer-
ebellum), spinocerebellum (paleocerebellum), and cerebrocer-
ebellum (neocerebellum) (Fig 2).
11
The oldest portion, the
vestibulocerebellum, primarily receives input fibers from the ves-
tibular system. The phylogenetically intermediate component,
the spinocerebellum, receives fiber input directly from the spinal
cord. The newest part, the cerebrocerebellum, receives input from
many different areas of the cerebral cortex. Interesting observa-
tions from fMRI studies, however, offer a different type of cere-
bellar organization based on function. Mapping of cognitive
functions shows a lateral cerebellar distribution, while the senso-
rimotor cerebellar functions are more medially located (
Fig 3).
12
This medial-to-lateral functional gradient also applies to the
group of 3 deep cerebellar nuclei (fastigial; interposed, consisting
of the globose and emboliform nuclei; and dentate). The cognitive
functions of the cerebellum, therefore, are primarily distributed
in the lateral aspect of the neocerebellum and ventral lateral aspect
of the dentate nuclei.
13
These same areas have shown an enor-
mous increase in size during hominid evolutionary development,
correlating with similar unusually large increases in prefrontal
and association cortices during the same phylogenetic period.
14,15
The mapping of associative learning with emotional, motor, and
cognitive functions also reveals a medial-to-lateral cerebellar dis-
tribution (
Fig 4).
16
Asymmetry of cerebellar functions is another interesting fea-
ture exposed by lesion and fMRI investigations. Language, for
instance, lateralizes to the right posterior cerebellar hemisphere
(in individuals who are left cerebral hemisphere language domi-
nant), and visuospatial function lateralizes to the left posterior
hemisphere.
17,18
Executive functions, however, seem to be bilat-
eral, while affective functions are primarily midline in the so-
called “limbic cerebellum” (
Fig 5). In addition, recent resting-
state
functional connectivity studies that explored functional
coupling showed asymmetrically organized cerebral cortical
networks in which functional coupling is stronger on one side
of the brain than the other. A fascinating corollary observation
is the parallel-though-reversed asymmetry of that functional
coupling in the cerebellum.
19
In other words, the cerebellum
not only reflects a homotopic map of the cerebral cortex but
also the asymmetric functional organization of the cerebrum.
These discoveries, therefore, not only demonstrate the novel
From the Medical College of Wisconsin, Department of Radiology, Neuroradiology
Section, Froedtert Hospital, Milwaukee, Wisconsin.
Please address correspondence to Leighton P. Mark, MD, Department of Radiol-
ogy, Neuroradiology Section, Froedtert Hospital, 9200 West Wisconsin Ave, Mil-
http://dx.doi.org/10.3174/ajnr.A4720
AJNR Am J Neuroradiol 37:1005– 09 Jun 2016 www.ajnr.org 1005
concept of nonmotor cerebellar functions but also a particular
set pattern of organization of those functions within the
cerebellum.
A closer examination of the functional maps of the cerebellum
reveals even greater levels of detailed organization.
20
The motor
tasks of the foot, hand, and face, for instance, demonstrate a so-
matotopic distribution predominantly at the medial aspect of the
anterior lobe of the cerebellum, but surprisingly, this same soma-
totopic relationship is also reflected in a mirror image fashion in
the posterior lobe (
Fig 6). When cerebellar maps of the cerebral
association
cortices are included on a sagittal view of the left cer-
ebellar hemisphere, several broad organizing principles become
evident (
Fig 7). Most of the cerebellum between the anterior and
posterior lobe motor areas maps to cerebral association areas.
20-23
The amount of cerebellum dedicated to a particular cerebral net-
work is proportional to the size of that cerebral network. In other
words, large cerebral networks are coupled to correspondingly
large cerebellar territories. The only exceptions are the primary
visual and auditory cortices, which are not represented in the
Lingula
Precentral fissure
Central lobule
Preculminate fissure
Primary fissure
Posterior superior fissure
VII A, Folium vermis
VII B, Tuber vermis
Horizontal fissure
Lobule HVII
Ansoparamedian fissure
Prepyramidal fissure
Secondary fissure
Flocculus
Posterolateral fissure
Pyramidal lobule
Uvula
Nodulus
Anterior lobe Posterior lobe Flocculonodular lobe
HII
HIII
Vermis
Hemisphere
I
II
III
IV
V
VI
VIII
IX
X
HX
HIX
HVIII
HIV
HV
HVI
Colmen
lobule
Simple
lobule
Crus I
of ansiform
lobule
Crus II
of ansiform
lobule
Paramedian
Biventer
Tonsil
I
VII
X
FIG 1. Unfolded view of the cerebellar cortex showing the lobes, lobules (by name on the right and number on the left), and main fissures (blue
font). The hemispheric lobules are designated with the prefix H followed by the Roman numeral indicating their corresponding vermian lobules.
Adapted from Haines DE. Fundamental Neuroscience for Basic and Clinical Applications. 4th ed. Philadelphia: Elsevier/Saunders; 2013 with
permission of Elsevier.
30
Spinocerebellum
Cerebrocerebellum
Vermis
Vestibulocerebellum
Nodulus
Flocculus
FIG 2. The cerebrocerebellum is the phylogenetically newest and
largest portion of the cerebellum. It primarily receives input indirectly
from many cerebral cortical areas. The spinocerebellum occupies the
median and paramedian zone of the cerebellum and receives input
directly from the spinal cord. The vestibulocerebellum is the phylo-
genetically oldest part of the cerebellum, and it receives input from
the vestibular nuclei of the brain stem. Adapted with permission from
Purves et al.
11
Deep Nuclei
Vermis
Hemispheric Lobules
Anterior
Lobe
Posterior
Lobe
NodulusFlocculus
Fastigial
Interposed
Dentate
I
II - III
IV
V
VIIa Crus I
VI
VIIa Crus II
VIIb
VIIIa
VIIIb
IX
Primary Fissure
Sensorimotor Cognitive
FIG 3. Unfolded view of the cerebellum illustrating sensorimotor-to-
cognitive functions distributed in a gradient-like fashion from medial
to lateral. The sensorimotor functions are distributed more toward
the midline, while the cognitive functions are located more laterally in
the cerebellar hemispheres. The same medial-to-lateral organization
is seen in the corresponding cerebellar nuclei. Adapted with permis-
sion from Fatemi et al.
12
1006 Klein Jun 2016 www.ajnr.org
human cerebellum. Figure 7 shows the primary cerebellar map
with motor functions in the anterior lobe followed by representa-
tions of premotor networks, executive control networks, and then
limbic-association networks, sometimes also referred to as the
default network. The secondary map continues around the cere-
bellum in reverse order with a flipped representation of the pri-
mary map. Crura I and II form the junction between the primary
and secondary maps. A map of the entire cerebellum also provides
an important overview (
Fig 8). Most of the human cerebellum
maps
to association areas rather than the motor cortex. Those
association areas also include executive control networks and the
default network. This pattern of distribution of cerebellar func-
tions implies that most of the cerebellum is coupled to nonmotor
functions paralleling the evolutionary development of the large
nonmotor portions of the cerebrum, prefrontal, and association
cortices.
Perhaps the most challenging basic issue for neuroradiologists
is accommodating to the novel and perhaps astonishing idea that
the cerebellum has fundamental cognitive and emotional func-
tions, let alone the equally astonishing proposal that most func-
tions of the cerebellum may be cognitive rather than motor in
nature. Considerable clinical evidence supports the concept of
cerebellar pathology associated with cognitive and psychiatric ill-
nesses. Schmahmann
24,25
was the first to propose the idea of a
“dysmetria of thought” due to cerebellar dysfunction. This con-
cept refers to the significant role of the cerebellum in sensory,
cognitive, and affective processing. The “cerebellar cognitive af-
fective syndrome” proposed by Schmahmann
26
has proved to be
clinically significant in disease recognition and understanding.
The litany of other psychiatric disorders now associated with cer-
Primary
fissure
Associative
learning
cognitive
motor
emotional
I
II, III
IV, V
VI
VIIIb
VIIIa
VIIb
VIIa
IX
X
Crus I, II
Lateral Intermediate Medial
FIG 4. Unfolded view of the cerebellum demonstrating associative
learning with emotional tasks located in the medial zone (yellow).
Motor tasks locate to the intermediate zone (orange), and cogni-
tive tasks occupy most of the cerebellar hemisphere in the lateral
zone (beige). Adapted from Timmann D, Drepper J, Frings M, et al. The
human cerebellum contributes to motor, emotional and cognitive
associative learning: a review. Cortex 2010;46:845–57 with permission
of Elsevier.
16
Left posterior
hemisphere:
visuospatial function
executive function
Posterior vermis:
affect and behavior
“limbic cerebellum”
Right posterior
hemisphere:
language function
executive function
FIG 5. Unfolded view of the cerebellum showing the asymmetric
distribution of some cerebellar functions. The right cerebellar hemi-
sphere is associated with language, and the left cerebellar hemi-
sphere, with visuospatial functions. Executive functions, including
verbal working memory, are related to both hemispheres. Attention is
also a neocerebellar function. The vermis or “limbic cerebellum” is
involved in modulating affective behavior. Adapted from Konczak J,
Timmann D. The effect of damage to the cerebellum on sensorimotor
and cognitive function in children and adolescents. Neurosci Biobe-
hav Rev 2007;31:1101–13 with permission of Elsevier.
17
FIG 6. A, Schematic demonstration of the cerebral and cerebellar
functional locations of the foot (green), hand (red), and face (blue) in
the monkey. B, Cerebellar locations of the foot (green), hand (red),
and tongue (blue) in humans measured by fMRI. “fcMRI” refers to
results based on functional connectivity studies. “Task” refers to re-
sults from task-based fMRI studies. C, Cerebellar locations of foot (F,
green), hand (H, red), and tongue (T, blue) representations in humans
from fcMRI studies displayed on a parasagittal image. Note the mirror
image representation of the somatomotor functions with the pri-
mary or dominant location in the anterior lobe of the cerebellum.
Adapted from Buckner RL. The cerebellum and cognitive function: 25
years of insight from anatomy and neuroimaging. Neuron 2013;80:
807–15 with permission of Elsevier.
31
AJNR Am J Neuroradiol 37:1005– 09 Jun 2016 www.ajnr.org 1007
ebellar pathology includes bipolar disorder, posttraumatic stress
disorder, attention deficit autism spectrum disorders, and schizo-
phrenia.
12,27
Many physicians, however, remain skeptical about
cognitive impairment due to cerebellar lesions. Part of this skep-
ticism may be due to the lack of sensitivity of most traditional tests
to evaluate cerebellar function because those tests were mostly
designed to detect motor abnormalities.
28
Another part may be a
lack of awareness/understanding of the precise nature of the more
nuanced functional abnormalities to look for on the clinical ex-
amination of cerebellar functions. Even so, not everyone is con-
vinced of cerebellar cognitive functions, and some effectively ex-
press a healthy skepticism.
29
For most neuroradiologists engaged
in fMRI studies, however, the cerebellar activation observed dur-
ing functional testing that was once dismissed as an aberration or
an exercise in technical rationalization should now be viewed with
a more critical eye.
The next Functional Vignette will review some of the impor-
tant anatomic pathways that correlate with the cognitive func-
tions of the cerebellum.
Disclosures: Vincent Mathews—UNRELATED: Grants/Grants Pending: GE Clinical
Trial,* National Institutes of Health,* Comments: both pending; Payment for Lec-
tures (including service on Speakers Bureaus): Eli Lilly, Comments: Amyvid Speakers
Bureau in 2013. *Money paid to the institution.
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map is hypothesized to be present in the posterior lobe as well.
Adapted from Buckner RL. The cerebellum and cognitive function: 25
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31
FIG 8. The 3 images on the left represent multiple coronal sections
of the cerebellum with colors representing different cortical func-
tions. The right-sided image is the cerebrum with the colors rep-
resenting the different functional areas. The somatomotor cortex
is blue. This cortex is represented at the more medial aspect of the
cerebellum. Most of the human cerebellum, however, is linked to
cerebral association networks, including executive networks (or-
ange) and the default network (red). These association networks
have multiple cerebellar representations. Adapted from Buckner
RL. The cerebellum and cognitive function: 25 years of insight from
anatomy and neuroimaging. Neuron 2013;80:807–15 with permis-
sion of Elsevier.
31
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AJNR Am J Neuroradiol 37:1005– 09 Jun 2016 www.ajnr.org 1009
