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T. J. H. Ruigrok
niques employing selective lesions of the spinal white matter
(Oscarsson and Sjolund 1977). As such it was established
that spinal afferents can affect olivary processing by way of
the ventral (or ventrolateral), (dorso-)lateral, and dorsal
funiculi (Fig.9.1b).
The ventral funiculus SOCP originates from several clusters of neurons located at the deeper layers of the contralateral cord and includes the lateral cervical nucleus. These
neurons relay mostly not only proprioceptive, but also cutaneous, information which, after crossing at segmental level
ascends just ventral to the ventral spinocerebellar tract to
reach the caudal part of contralateral medial accessory and
entire dorsal accessory olive. Olivocerebellar axons from the
caudal halves of the accessory olives again cross the midline
to reach the cerebellum by way of the inferior cerebellar
peduncle to terminate unilaterally in A and B zones of the
vermis (caudal parts of medial and dorsal accessory olives,
respectively) or in the paravermal C1 and C3 zones (rostral
part of the dorsal accessory olive) of the spinocerebellum.
A second pathway from the spinal cord to the inferior
olive uses the dorsal funiculus and relays at the dorsal column nuclei (DFSOCP). At least part of this pathway originates from neurons from the deeper layers of the dorsal horn
and is also referred to as the postsynaptic dorsal column
pathway to the inferior olive. Available evidence suggests
that the postsynaptic dorsal column pathway originates from
different spinal sources and mediates less sensitive and/or
nociceptive signals to the inferior olive as compared to the
direct spino-olivary route (Flavell etal. 2014).
Finally, the third spino-olivocerebellar route passes
mostly through the ipsilateral lateral funiculus and relays
through several, as yet not further specied, brainstem intermediaries before activating the contralateral inferior olive
(i.e., rostral part of the medial accessory and the principal
olives) that supply climbing bers to the C2 and D1 zones
(Voogd etal. 2022).
SOCPs can activate climbing bers of all major cerebellar
zones (excepting those of the vestibulocerebellum) but do so
with different latencies (Lawrenson etal. 2016). Transmission
within the SOCPs varies within, e.g., different phases of the
stepcycle (Lidierth and Apps 1990).
9.2 Information Routes
fromtheCerebellum totheSpinal
Cord
the cerebellum may control several autonomic descending
pathways (Fujita etal. 2020; Zhu etal. 2006), we will concentrate on the cerebellar control of pathways that are mostly
involved in motor control. Classically, these are separated
into medial descending systems, which course through the
ventral funiculus and lateral descending systems, which pass
the lateral funiculus (Lawrence and Kuypers 1968). Medial
systems comprise the uncrossed medial corticospinal tract
and the tectospinal, vestibulospinal, reticulospinal, and interstitiospinal pathways. The lateral systems involve the crossed
corticospinal tract and the rubrospinal tract. In addition, the
cerebellum itself may directly control spinal processing.
9.2.1 Lateral Systems
9.2.1.1 The Crossed Corticospinal Tract
The crossed corticospinal tracts originates mostly from the
primary motor (area 4), premotor (area 6) and, to a lesser
extent, from somatosensory cortices (areas 1–3). As output
from all cerebellar nuclei will reach the ventral lateral and
ventral anterior parts of the thalamus (i.e., the classic “motor”
thalamus), but not the ventral posterior nucleus, cerebellar
processing will be important for voluntary movement control
as directed by primary and secondary motor cortices
(Fig.9.1c). Presently, it is debated to what extent cerebellar
output is involved in corticospinal information processing
within somatosensory cortical regions (Aoki et al. 2019;
Proville etal. 2014; Schafer and Hoebeek 2018).
9.2.1.2 The Rubrospinal Tract
The rubrospinal tract originates from the magnocellular part
of the red nucleus. Its bers cross at the level of the nucleus
and descend in the ventrolateral medulla to take up position
in the lateral funiculus just ventral to, and partly intermingled with, the bers from the crossed corticospinal tract.
Although in most mammals the tract terminates throughout
the spinal cord, its contribution to cervical processing seems
to have increased in animals with reaching capacities of their
forelimbs. However, in higher primates the importance of the
rubrospinal tract seems to have degraded as in man only a
few hundred rubrospinal bers are described that may not
even reach caudal cervical levels (Onodera and Hicks 2009).
The rubrospinal tract is under the exclusive control of the
anterior interposed nucleus (i.e., C1 and C3 cortical zones;
Fig.9.1c) (Voogd etal. 2022).
From the brain arises a multitude of pathways that descend
to the spinal cord. Many of these can be inuenced by output
from the cerebellum. As the cerebellar nuclei constitute the
main output station of cerebellar processing, the organization of their output will determine how the cerebellum inuences these descending pathways and spinal cord. Although
9.2.2 Medial Systems
9.2.2.1 The Uncrossed Corticospinal Tract
The origin of the uncrossed corticospinal tract seems to be
similar to that of the crossed corticospinal tract. However,
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caudal to the pyramidal decussation, it takes an ipsilateral
route through the ventral funiculus to terminate predominantly contralaterally on interneurons in the medial part of
the ventral horn (Fig.9.1c). Cerebellar control is likely to be
similar to that of the crossed corticospinal tract.
9.2.2.2 The Tectospinal Tract
The superior colliculus is involved in directing gaze to
objects of interest by inducing saccades, head movements, or
a combination of both. However, arm or even whole body
movements may also be evoked by its stimulation. As such,
it has been suggested to control reexive behaviors such as
defensive and orienting behavior. The tectospinal tract, arising from large cells in the deeper layers of the caudolateral
part of the superior colliculus mostly decussates in the dorsal
tegmental tract and descends in the ventral funiculus but
does not project beyond the cervical segments from where
the neck muscles are innervated (Nudo and Masterton 1989).
Tectospinal bers also have ample brainstem collaterals,
which can affect cervical muscles by way of reticulospinal
pathways (Isa etal. 2020).
Cerebellar output from the fastigial, posterior interposed
and lateral cerebellar nucleus reaches predominantly the
deeper layers of the superior colliculus. As such, all these
regions are likely to inuence tectospinal processing (NiemiJunkola and Westby 2000).
9.2.2.3 The Vestibulospinal Tracts
The vestibular nuclear complex, classically divided into a
medial, spinal, lateral, and a superior vestibular nucleus, is
intimately and reciprocally connected with the cerebellar
cortex as well as its nuclei. Indeed, the vestibular complex is
special because it is the only brainstem system that receives
afferents from the cerebellar nuclei as well as directly from
the cerebellar cortex. Descending output of the vestibular
nuclei is directed to the spinal cord by way of the medial and
lateral vestibulospinal tracts (Fig.9.1c), which are involved
in balance and antigravitational control.
The medial vestibulospinal tract descends by way of the
medial longitudinal fascicle, entering and coursing in the
ventral funiculus at its dorsal aspects. Fibers of the medial
vestibulospinal tract originate from the ipsilaterally located
inhibitory neurons and from excitatory, but contralaterally
located vestibular neurons. The medial tract terminates bilaterally in the ventromedial aspects of the spinal grey where
they have both inhibitory and excitatory actions on their
postsynaptic targets. The medial tract does not seem to
descend beyond midthoracic levels and mostly inuences
motoneurons that innervate neck and axial musculature
(Fig.9.1c).
Vestibular neurons contributing to the medial vestibulospinal tract may receive information from either the medial
cerebellar nucleus or from Purkinje cells of the vestibulocer-
ebellum (occulus and nodulus) that project directly to the
vestibular nuclei. The rostral part of the medial cerebellar
nucleus, receiving input from the vermal A zone (Voogd
et al. 1996), projects by way of the superior cerebellar
peduncle to the ipsilateral medial vestibular nucleus. The
same area is also reached by the contralateral medial cerebellar nucleus by way of the uncinate tract that crosses in the
cerebellar commissure. In mice, the ipsilateral nucleovestibular connections are glycinergic, whereas the contralateral projections are glutamatergic, suggesting that the
cerebellum can exert a push–pull mechanism on balancing/
posturing control (Bagnall etal. 2009).
The lateral vestibulospinal tract originates from the ipsilateral lateral vestibular nucleus (Deiters’ nucleus), is excitatory, and descends by way of the anterolateral fascicle to
thoracic levels of the cord where it shifts more toward the
ventral funiculus. The lateral tract terminates throughout the
length of the cord in the ventromedial laminae of the spinal
grey (lamina VII–VIII: Fig.9.1c), and may make direct synaptic contacts with motoneurons that control anti-gravity
muscles (Arshavsky etal. 1986). The main afferent source of
the lateral vestibular neurons is the axons of the Purkinje
cells of the B zone that is found in the lateral vermis of the
anterior lobe and lobule VIII.Indeed, as most lateral vestibular neurons are active during the stance phase of locomotion,
it was shown that cooling of the anterior cerebellar vermis
results in prolonged stance phases (Arshavsky etal. 1986;
Udo etal. 1976).
9.2.2.4 The Reticulospinal Tracts
Many regions in the medial and medioventral pontomedullary reticular formation are at the origin of several long
descending tract systems travelling ipsilaterally in a medial
(mostly from pontine levels) and bilaterally in ventral and
ventrolateral reticulospinal tracts (mostly from medullary
levels: Fig. 9.1c) (Newman 1985a, b; Torvik and Brodal
1957). Many bers provide collaterals to cervical as well as
lumbar levels. Reticulospinal systems have been described
as subserving many different functions as they are involved
in maintaining and controlling ongoing motor activity (e.g.,
Esposito etal. 2014), in the gating of somatosensory information to segmental as well as supraspinal levels, and in the
control of autonomic activity including pain modulatory systems (Fields 2004). Four regions of the cerebellar nuclei supply projections to the reticular formation and, as such, may
inuence processing in reticulospinal systems.
Detailed functional control of the medial cerebellar
nucleus on reticulospinal pathways has been provided by
Fujita et al. (2020). In general, the caudal aspect of the
medial cerebellar nucleus, which is specically targeted by
vermal oculomotor areas of lobules VI and VII, projects contralaterally to the medial pontine reticular formation as well
as to the dorsomedial medullary reticular formation which
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seem to be mostly involved in control of eye and neck movements, respectively. More intermediate and dorsolateral parts
of the medial nucleus reach intermediate and lateral (i.e.,
parvocellular) parts of the contralateral reticular formation.
The rostral part of the medial nucleus, although mostly supplying terminals to the vestibular nuclei, also projects to
intermediate (mediolateral) levels of the reticular formation
and to the lateral paragigantocellular nucleus. Specic
regions of the medial cerebellar nucleus may be involved in
the control of several autonomic functions including control
of cardiovascular reexes (Fujita et al. 2020; Nisimaru
2004).
In the rat, several cell groups, intercalated between the
medial and the interposed nuclei, are the target of the
Purkinje cells of the X and CX zone (Buisseret-Delmas etal.
1998). They have been shown to have projections to selective
regions of the contralateral pontomedullary reticular formation, such as the gigantocellular reticular nucleus. However,
the interstitial cell groups also supply afferents to the
vestibular nuclei and the interstitial nucleus of Cajal. In
rodents, furthermore, a prominent ipsilateral projection
emerges from the enlarged lateral part of the anterior interposed nucleus, termed the dorsolateral hump, and which
supplies afferents not only to the parvicellular regions of the
ipsilateral pontomedullary reticular formation but also
invades the deeper layers of the spinal trigeminal nucleus.
Stimulation evokes movements of lips, neck, and forelimb
(Cicirata et al. 1992). The dorsolateral hump receives its
Purkinje ber input from the D0 zone, which is intercalated
between the D1 and D2 zones of lobules V–VII. It is not
known if a primate equivalent exists.
Finally, the connections of the lateral nucleus with the
pontomedullary reticular formation are well documented for
rodents, cats, and monkey and are particularly dense to the
contralateral gigantocellular reticular nuclei (Fig. 9.1c)
(Kebschull etal. 2020; Teune etal. 2000). The projection
originates mostly from the dorsal, magnocellular, aspects of
the nucleus and has been shown to activate reticulospinal
neurons monosynaptically (Tolbert etal. 1980). The role of
this disynaptic dentate-reticulo-spinal connection is not yet
clear.
9.2.2.5 The Interstitiospinal Tract
The interstitiospinal tract originates from a region with scattered large neurons located within and surrounding the
medial longitudinal fascicle at midbrain levels, and which is
known as the interstitial nucleus of Cajal. This region is
known to be involved in oculomotor control but at least some
of its bers descend ipsilaterally by way of the ventral funiculus to the spinal cord where they terminate in laminae VII
and VIII of the spinal gray. It has been suggested to be
involved in orienting behavior (Fujita etal. 2020). The inter-
stitiospinal tract has not only excitatory monosynaptic contacts with neck musculature but also provides di- and
polysynaptic, mostly excitatory, activation of back, fore-,
and hindlimb muscles (Fukushima etal. 1978; Holstege and
Cowie 1989). Cerebellar projections to the interstitial nucleus
of Cajal arise predominantly from the medial cerebellar
nucleus, but other cerebellar nuclear areas also contribute.
9.2.3 Direct Cerebellospinal Projections
Although the cerebellum exerts its inuence on descending
pathways primarily by its nuclear projections to the brainstem and diencephalon, some cerebellar nuclear efferents
also reach the spinal cord directly. Classical studies in cat
determined that cerebellar projections, arising mostly from
the contralateral medial and medial interposed cerebellar
nuclei did not descend beyond high cervical levels
(Matsushita and Hosoya 1978). Recent studies, however,
show that, in mice, a more prominent bilateral direct spinal
control can be exerted by neurons located in the medial and
interposed nuclei. Spinal projections to cervical as well as
lumbosacral level originate from the ipsilateral anterior
interposed nucleus, whereas contra- as well as ipsilateral
connections to the cervical cord are reported to arise from
both interposed as well as from the medial cerebellar nucleus
(Fig.9.1c). The ispi- and bilaterally descending direct spinal
projections may be differentially controlling motor performance and motor learning, respectively (Sathyamurthy etal.
2020).
9.3 Conclusion
The cerebellum is widely known as a structure with a uniform internal circuitry that processes information in a stereotypic way. Within the internal circuitry, a number of
parasagittally organized modules are recognized which form
functional entities (Apps and Hawkes 2009; Ruigrok 2011).
The organization of the input to these modules and the organization of their output channels, therefore, will determine
the type of information processed within such a cerebellar
module and which structures will be informed of its result.
The overview presented in this chapter demonstrates that
detailed knowledge of the spino-cerebellar and cerebellospinal connections with these modules is still not at a level
that enables a deeper understanding of cerebellar functions.
A detailed description of the interaction of the various spinocerebellar systems with the cerebellar modular circuitry is
required together with an improved perception of how the
output of modules is distributed to the centers from which
descending tracts originate.
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Visual Circuits
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ManuelJanRoth, AxelLindner, andPeterThier
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Abstract
The cerebellum receives substantial input from visual and
eye movement-related areas through the pontine nuclei.
These signals are used to guide and rene motor behavior
and to establish spatial orientation. Accordingly, damage
to the cerebellum can lead to imprecise eye movements
and decits in visual perception. Here, we discuss these
cerebro-cerebellar circuits supporting vision.
Keywords
Cerebellum · Cerebellar anatomy · Eye movements
Visual perception · Sensory predictions · Forward
models
10.1 Anatomical Considerations
Visual information processing in the cerebrum engages various areas that make up a large amount of the cerebral cortex.
Many of these areas also project to the cerebellum. There,
visual information, in combination with other inputs such as
vestibular signals, is integrated in order to inform spatial orientation and to (visually) guide and rene motor behavior,
such as eye movements (Thier 2011).
To allow for such close interaction, both cerebral and cerebellar cortices must share information. Hence, it is not surprising that the extensive projection system connecting these
two structures by way of the pontine nuclei constitutes one of
the largest circuits in the human brain. Information from sensory and motor areas of the cerebral cortex, which account
for the largest portion of pontine afferents, and also from
additional subcortical structures such as the superior colliculus (Glickstein 2013; Schwarz and Thier 1999), enters the
cerebellum mainly via the pontine nuclei (PN) and other precerebellar nuclei such as the nucleus reticularis tegmenti
pontis (NRTP), which will not be discussed here.
The PN are located below the cerebral peduncles in the
ventral portion of the pons and are subdivided into several
nuclei based on their cytoarchitecture and their general location. They consist of roughly 20,000,000 neurons, accounting for almost 40% of pontine brainstem volume (Matano
etal. 1985; Tomasch 1969). A large majority of these neurons are considered projection neurons connecting the cerebral and cerebellar cortex (Cooper and Fox 1976). Because
of its intermediate position between the two cortices receiving not only cerebrocortical but also collicular visual and eye
movement-related signals (see Thier and Möck 2006 for
review), the PN are believed to be an important integrative
relay of the visual and eye movement pathways on which we
focus here.
M. J. Roth · A. Lindner
Department of Cognitive Neurology, Hertie Institute for Clinical
Brain Research, University of Tübingen, Tübingen, Germany
Department of Psychiatry and Psychotherapy, Tübingen Center for
Mental Health (TüCMH), University Hospital of Tübingen,
Tübingen, Germany
e-mail: a.lindner@medizin.uni-tuebingen.de
P. Thier (*)
Department of Cognitive Neurology, Hertie Institute for Clinical
Brain Research, University of Tübingen, Tübingen, Germany
e-mail: thier@uni-tuebingen.de
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
D. L. Gruol et al. (eds.), Essentials of Cerebellum and Cerebellar Disorders, https://doi.org/10.1007/978-3-031-15070-8_10
10.1.1 Cerebrocortical Areas Projecting
tothePons
Using retrograde tracers injected into the PN to study the
distribution and density of corticopontine projections,
Glickstein and colleagues found labeled layer 5 pyramidal
cells within a contiguous region covering parts of frontal,
parietal, and temporal lobe (Glickstein et al. 1985;
Fig.10.1a). More precisely, the region containing substantial
numbers of labeled cells ranged from the insular cortex
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d1
d2 d3 d4
Fig. 10.1 (a) Cortical region (shaded areas) that has been found to
project to the PN using retrograde tracers in a monkey. Layer 5 pyramidal cells (black dots) within a region involving parts of frontal, parietal,
and temporal lobe, ranging from the insular cortex within the sylvian
ssure laterally to the ventral edge of the cingulate cortex medially and
from the arcuate sulcus rostrally to the superior temporal sulcus caudally project to the PN (modied from Glickstein et al. 1985). (b)
Schematic drawing of a caudal view of cerebellar cortex with the location of the two main oculomotor regions highlighted. The oculomotor
vermis (OMV) is shown in blue and the dorsal paraocculus in red
(adapted from Thier and Möck 2006). (c) Exemplary data on visually
guided saccades of a cerebellar patient (empty circles) and a control
subject (dark grey dots). Note the wide spread of saccade endpoints of
the patient (dysmetria) compared to the control (modied from Golla
etal. 2005). (d) Performance in smooth pursuit of a patient suffering
from cerebellar degeneration compared to a healthy control group. (d1)
Eye movement traces (red lines) in a task where the subject was supposed to track a moving target at 8°/s (black line). The pursuit velocity
is insufcient to stay on the target, which leads to compensatory corrective saccades. (d2–d4) Psychophysical evidence for impaired visual
analysis of a moving object (d2) as a result of smooth pursuit decits
(d3–d4) in a cerebellar patient (empty circles) compared to a healthy
control group (modied from Haarmeier and Thier 1999). DPF dorsal
paraocculus, FL occulus, PML paramedian lobule
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within the sylvian ssure laterally to the ventral edge of the
cingulate cortex medially and from the arcuate sulcus rostrally to the superior temporal sulcus caudally (Brodmann’s
areas 1–10, 13, 14, 19, 23–25; Brodmann 1909).
Importantly, this contiguous region comprises all parts of
cortex contributing to the control of movement and to spatial
orientation, among others. These areas include the frontal eye
elds (FEF; Bruce etal. 1985; Gottlieb etal. 1994), supplementary eye elds (SEF, Heinen 1995; Schlag and SchlagRey 1985, 1987), lateral intraparietal (LIP) and medial
parietal areas (MP; Andersen etal. 1990; Barash etal. 1991a,
1991b; Thier and Andersen 1997, 1998), medial superior
temporal area (MST; Kawano et al. 1994; Newsome and
Wurtz 1988; Thier and Erickson 1992), and middle temporal
area (MT; Dursteler and Wurtz 1988; Newsome etal. 1988).
Further analyses of the cerebro-pontine projections of these
regions showed that most of them terminate in the dorsal part
of the ipsilateral PN within several elongated lamellae that
often span several subnuclei (Schmahmann and Pandya 1989,
1993). This suggests that the cytoarchitectonic subdivision of
the PN into several nuclei does not correspond to the organization of afferent terminations (Thier and Möck 2006).
10.1.2 Pontocerebellar Projections
andCerebellar Output
The axons of pontine projection neurons enter the cerebellum by way of the middle cerebellar peduncle and terminate
as mossy bers in the granular layer of the cerebellar cortex.
Granular cells in turn give rise to the parallel bers, which
connect to Purkinje cells which are the only output neurons
of the cerebellar cortex. While most of the pontocerebellar
bers terminate in the contralateral part of the cerebellum,
there seem to be also ipsilateral projections (Rosina et al.
1980). Major projection sites of these neurons that show
involvement in eye movements and will be discussed in the
following section are lobuli VII and VIc of the posterior vermis, the caudal vermis as well as the neighboring dorsal
paraocculus (Thier 2011; Fig.10.1b).
Visual and eye movement-related signals leave the cerebellum through the projection of Purkinje cells to the deep
cerebellar nuclei (DCN). The major targets of eye movementrelated signals are the caudal fastigial and the posterior interposed nuclei (Sun etal. 2016; Thier 2011).
10.2 Cerebellum andEye Movements
The cerebellum is of utmost importance for visual perception because it optimizes goal-directed eye movements such
as saccadic and smooth pursuit eye movements that inu-
ence how and where visual information is actively acquired.
Moreover, ocular reexes such as the vestibulo-ocular reex
(VOR) or the ocular following response (OFR) contribute to
the stabilization of visual perception despite the movements
of the observer (Dash and Thier 2014; Thier 2011). The ability to precisely direct gaze toward objects of interest as well
as to perceive a stable visual world despite one’s own movements lies at the heart of the visual perceptual abilities we are
capable of. At this point, it is important to note, however, that
the cerebellum is of course not only involved in directing and
optimizing eye movements. Rather it contributes to any form
of sensory guided movement such as limb movements
(Bastian 2011).
10.2.1 Cerebellar Lesions Impair Saccades
andSmooth Pursuit Eye Movements
Saccades are fast and goal-directed eye movements that
serve to bring the image of an object of interest onto the
fovea, i.e., the part of the retina that accommodates the
highest visual acuity. Being able to perform precise saccades is important for ensuring proper object analysis. In
cases in which an object of interest is moving and/or the
observer is moving, smooth pursuit eye movements are
additionally engaged to track the object by matching eye
velocity to target velocity and thereby keeping it on the
fovea (often supported by additional head and body
movements).
Immediate insights into the importance of the cerebellum for eye movements are provided by lesion studies.
Barash and colleagues showed that after lesioning small
parts of the oculomotor vermis in macaque monkeys,
visually guided saccades became hypometric, i.e., saccades fell too short relative to the saccade target (Barash
etal. 1999). While the hypometria disappeared over time,
saccadic endpoints remained imprecise, arguably forever.
Similarly, also human subjects suffering from cerebellar
damage involving the posterior vermis exhibit saccades
characterized by variable endpoints (Golla et al. 2005;
Fig.10.1c). An analogous loss of precision is exhibited by
smooth pursuit eye movements (Takagi etal. 2000). While
healthy subjects are capable of smoothly tracking a constantly moving visual target, patients with cerebellar damage and animals with experimental lesions fail in doing
so. This is because their eye velocity is typically too small
to match target velocity. Therefore, the distance between
the tracked object and the fovea continuously increases
during the course of a tracking movement and this “foveation error” then needs to be repeatedly compensated by
subjects with “catch-up” saccades (Haarmeier and Thier
1999; Fig.10.1d).
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10.2.2 Cerebellar Adaptation ofEye
Movements
As we have seen in the previous paragraph, damage to specic parts of the cerebellum causes imprecise visually guided
eye movements. The role of the cerebellum thus seems to be
the optimization of these movements. Compromised precision is not only conned to visually guided eye movements
but also other forms of sensory-guided motor behavior
(“ataxia”; Markanday etal. 2018).
The cerebellar role in rening motor output is a direct consequence of its ability to adjust key parameters characterizing
the necessary sensorimotor transformations as revealed in
typical adaptation paradigms. As said before, in the study by
Barash and colleagues, the hypometric saccades of monkeys
with vermal lesions returned to pre-lesion amplitudes after a
few weeks, although displaying larger endpoint variations.
What was completely abolished, however, was the capacity to
adapt saccade amplitudes in a short-term adaptation paradigm, requiring modications of saccade amplitude in order
to compensate intrasaccadic shifts of target position (Barash
etal. 1999). This nding agrees with a large body of literature
describing adaptation decits of saccades and smooth pursuit
due to cerebellar disease and experimental lesions in animals,
respectively (e.g. Straube et al. 2001; Takagi et al. 1998).
Analogous decits have also been reported for skeletomotor
movements in tasks that call for an adaptation of motor output
in response to altered sensorimotor relationships [e.g. prism
adaptation (Martin etal. 1996)]. In fact, decits in adaptation
or motor learning are key symptoms of patients suffering
from cerebellar damage (Bastian 2011).
Adaptation decits revealed in experimental settings
reect the capacity of the cerebellum to continuously recalibrate motor output in order to ensure optimal motor behavior. Hence, the occurrence of imprecise visually guided eye
movements hand in hand with a loss of the ability to adapt
them have the same mechanistic basis. A major inuence
calling for recalibration on a short time scale is “fatigue,” a
loss of the vigor of movement not only due to use-dependent
changes of the movement effectors (Prsa etal. 2010), but
also due to a loss of motivation and attention to the movement (Markanday etal. 2018). Thus, vermal pathology also
causes the inability to compensate changes due to fatigue
(Golla etal. 2008).
Motor output recalibration or motor updating is believed
to depend on “forward models” which predict the sensory
consequences of movements on the basis of motor commands and (sensory) information about the current state of
the system. Using these predictions, movements can be corrected on the y and no longer depend on delayed sensory
feedback errors, thereby guaranteeing fast and accurate
movements (Wolpert and Ghahramani 2000). There is now
broad agreement that the role of the cerebellum can be traced
back to its ability to predict the sensory consequences of
movements and to ensure that forward model predictions are
precisely tuned (Bastian 2006; Wolpert etal. 1998).
10.3 Cerebellar Contributions toVisual
Perception
Precise eye movements are needed to make full use of visual
information for perception. Hence, the cerebellum clearly
serves visual perception, yet indirectly, namely through its
central role in optimizing motor output. However, does it
also have a direct inuence on visual perception? In the following sections, we will focus on direct cerebellar contributions to vision, some of which seem independent of eye
movements. We argue that these contributions can be traced
back to the same computational principle that contributes to
motor behavior, namely the optimization of predictions
within the framework of forward modelling.
10.3.1 A Role oftheCerebellum inGlobal
Visual Motion Perception
A visual decit not explainable by insufcient eye movements that has been consistently reported over the last years
is a decit in detecting a global visual motion component
embedded in randomly moving dots (Händel et al. 2009;
Jokisch et al. 2005; Nawrot and Rizzo 1995; Thier et al.
1999). Compared to healthy controls, cerebellar patients
need a much higher degree of coherently moving dots within
a moving random dot pattern to establish a global visual
motion percept (Fig.10.2a). The reason behind this decit is
most likely that parietooccipital processing of motion signals
in area MT and neighboring areas of parietooccipital cortex
is corrupted, arguably due to a loss of essential functional
input from the cerebellum (Händel etal. 2009). Indirect support for this pathway stems from experiments in nonhuman
primates, which show that electrical microstimulation of the
deep cerebellar nuclei gives rise to activity in motion processing cortex (Sultan etal. 2012). Furthermore, cerebellar
bers indirectly contacting motion processing areas thought
to be homologous to primate area MT were also found in the
cat (Sasaki etal. 1972; Wannier etal. 1992).
The need for cerebellar input to motion processing cortex
may be based on the fact that visual motion on the retina can
be caused by both motion in the environment and by egomotion. In order to extract the respective contributions of
these different motion signals, each of which is relevant for
different types of behavior, the visual system resorts to predictions about the visual consequences of performed egomotion (Haarmeier etal. 2001; von Holst and Mittelstaedt
1950). Specically, the predicted motion information is
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Fig. 10.2 (a) Decits of a cerebellar patient suffering from spinocer-
ebellar ataxia type 6 (SCA6) in global visual motion perception. When
measuring the percentage of coherently moving dots necessary to evoke
a percept of global motion in a display of otherwise randomly moving
dots, this SCA6 patient (light grey bar) has not only a strongly elevated
threshold compared to a healthy population (red line), but her perceptual threshold is in fact closer to the one of a motion blind patient due to
cortical lesions; data from (Scherer, Thier & Haarmeier, unpublished
data; Zihl etal. 1983). (b) Depiction of a forward model used to predict
and perceptually cancel self-induced motion of the world during smooth
pursuit eye movements. If one is tracking a moving object with the eyes
in order to stabilize its retinal image, a motor command is generated to
achieve this desired state (specication of movement). At the same
time, the system uses this motor command to form a prediction about
the sensory outcome of the respective behavior (predicted state). This
attributed as self-produced, whereas any residual (not predicted) motion information is interpreted as externally
caused (Fig.10.2b). And it is the cerebellum that is responsible for generating this prediction and for keeping it optimal
based on forward modelling (Lindner etal. 2006). Thus, it
prediction can then be used for feed-forward movement control (dotted
lines), but also to cancel self-caused retinal motion of the world (dashed
lines; adapted from Lindner et al. 2005). (c) Decit of cerebellar
patients in recalibrating a spatiotemporal prediction in response to
altered stimulus statistics. (c1) Subjects had to predict the time of reappearance of a constantly moving visual target that transiently disappeared behind an occluder. The time the visual target spent behind the
occluder was manipulated in such a way, that– as compared to a baseline condition– the target reappeared consistently too late. (c2) While
healthy controls recalibrated their prediction about when the target
should reappear in response to the target reappearing too late, as indicated by a shift of the psychometric function toward more positive
delays (dT), cerebellar patients did not show such a pronounced recalibration (adapted from Roth etal. 2013)
could be the loss of such a precise “reference signal” that
may clutter motion processing in cerebral cortex– even in
the absence of ego motion.
Also, from a theoretical point of view, such sensory predic-
tions or forward models need to undergo constant recalibration
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