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Prolonged rock climbing activity induces structural changes in cerebellum and parietal lobe

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  • University of Rome Tor Vergata and IRCCS Fondazione Santa Lucia , Roma
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Prolonged rock climbing activity induces structural changes in cerebellum and parietal lobe

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This article analyzes whether climbing, a motor activity featured by upward movements by using both feet and hands, generation of new strategies of motor control, maintenance of not stable equilibrium and adoption of long-lasting quadrupedal posture, is able to modify specific brain areas. MRI data of 10 word-class mountain climbers (MC) and 10 age-matched controls, with no climbing experience were acquired. Combining region-of-interest analyses and voxel-based morphometry we investigated cerebellar volumes and correlation between cerebellum and whole cerebral gray matter. In comparison to controls, world-class MC showed significantly larger vermian lobules I-V volumes, with no significant difference in other cerebellar vermian lobules or hemispheres. The cerebellar enlargement was associated with an enlargement of right medial posterior parietal area. The specific features of the motor climbing skills perfectly fit with the plastic anatomical changes we found. The enlargement of the vermian lobules I-V seems to be related to highly dexterous hand movements and to eye-hand coordination in the detection of and correction of visuomotor errors. The concomitant enlargement of the parietal area is related to parallel work in predicting sensory consequences of action to make movement corrections. Motor control and sensory-motor prediction of actions make the difference between survive or not at extreme altitude. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.
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rHuman Brain Mapping 34:2707–2714 (2013) r
Prolonged Rock Climbing Activity Induces
Structural Changes in Cerebellum and
Parietal Lobe
Margherita Di Paola,
1,2
*Carlo Caltagirone,
1,3
and Laura Petrosini
1,4
1
IRCCS Santa Lucia Foundation, Via Ardeatina 306, 00179 Rome, Italy
2
Department of Internal Medicine and Public Health, University of L’Aquila,
Piazzale Salvatore Tommasi 1, 67010 L’Aquila – Coppito, Italy
3
Department of Neuroscience and Memory Clinic, ‘‘Tor Vergata’’ University of Rome,
Via Montpellier, 1 00133 Rome, Italy
4
Department of Psychology, University ‘‘Sapienza’’ of Rome, Via dei Marsi, 78, 00185 Rome, Italy
r r
Abstract: This article analyzes whether climbing, a motor activity featured by upward movements by
using both feet and hands, generation of new strategies of motor control, maintenance of not stable equi-
librium and adoption of long-lasting quadrupedal posture, is able to modify specific brain areas. MRI
data of 10 word-class mountain climbers (MC) and 10 age-matched controls, with no climbing experience
were acquired. Combining region-of-interest analyses and voxel-based morphometry we investigated cer-
ebellar volumes and correlation between cerebellum and whole cerebral gray matter. In comparison to
controls, world-class MC showed significantly larger vermian lobules I-V volumes, with no significant
difference in other cerebellar vermian lobules or hemispheres. The cerebellar enlargement was associated
with an enlargement of right medial posterior parietal area. The specific features of the motor climbing
skills perfectly fit with the plastic anatomical changes we found. The enlargement of the vermian lobules
I–V seems to be related to highly dexterous hand movements and to eye-hand coordination in the detec-
tion of and correction of visuomotor errors. The concomitant enlargement of the parietal area is related
to parallel work in predicting sensory consequences of action to make movement corrections. Motor con-
trol and sensory-motor prediction of actions make the difference between survive or not at extreme alti-
tude. Hum Brain Mapp 34:2707–2714, 2013.V
C2012 Wiley Periodicals, Inc.
Key words: word-class rock climbers; cerebellum; cerebral cortex; region of interest; voxel-based
morphometry
r r
INTRODUCTION
Climbing is a complex motor activity in which the sus-
tained vertical motion, and the peculiar role of upper
limbs, distinguishes it from other land-based movements
[Quaine and Martin, 1999]. The activity is characterized by
short bouts of high-intensity exercise, with short intermit-
ted periods of rest. The upper body checks the posture,
while the lower limbs are mainly involved in sustaining
the body mass [Bourdin et al., 1998]. Besides the produc-
tion of these voluntary motor activities, climbing requires
motor learning of new motor schemes, coordination of the
body parts involved in the vertical movement (synergia),
and ability to carry out rapidly the voluntary movements
in successive sequences (diadochokinesis) in order to keep
the body in balance. For human beings, indeed, moving
*Correspondence to: Margherita Di Paola, IRCCS Santa Lucia
Foundation, Via Ardeatina 306, 00179 Rome, Italy.
E-mail: m.dipaola@hsantalucia.it
Received for publication 11 January 2012; Revised 29 February
2012; Accepted 16 March 2012
DOI: 10.1002/hbm.22095
Published online 21 April 2012 in Wiley Online Library
(wileyonlinelibrary.com).
V
C2012 Wiley Periodicals, Inc.
vertically requires per se a motor learning. Additionally, it
has been found [Zampagni et al., 2011] that expert climbers
acquire two adaptive features. More in details, they adopt
and well manage a peculiar motor pattern consisting in a
paradoxical ‘‘destabilization’’ of the center of mass (COM)
oscillations in the lateral direction and surprisingly large
distances of the body from the vertical structure. Moreover,
during climbing in order to keep the body in balance,
upward center of mass COM displacements are prevalently
guaranteed by the greater vertical forces generated onto the
feet’s support, whereas the forces onto the hands act much
more in overhanging position [Noe, 2006; Noe and Quaine,
2006; Noe et al., 2001]. As it is known, the cerebellum is
organized into functional divisions with distinct connections
to the brain and spinal cord. The vestibulocerebellum con-
trols balance and eye movements, spinocerebellum adjusts
on-going movements and cerebrocerebellum coordinates
the planning of movements [Glickstein et al., 2009]. Further-
more, cerebellum has been considered a region largely
involved in motor learning [Manto and Jissendi, 2012]. All
together, the cerebellum appears not only strongly impli-
cated in the control of movement but simultaneously it
appears to have functions that go beyond this control. Its
role in motor learning is continuously required because nor-
mal motor behavior and even more motor complex learned
activity which require constant adaptation as circumstances
change. Thus, in this study investigating the relation
between a motor complex learned activity, such as climb-
ing, and cerebellar macrostructural changes appeared par-
ticularly appropriate.
Experimental studies suggest a causal relationship
between motor skill learning, exercise and structural
changes of cerebellar structures [Anderson et al., 2002;
Kleim et al., 1997]. Also human studies demonstrate that
learning-induced neuroplasticity is reflected at a structural
level in brain areas demanded by the practiced task [Bez-
zola et al., 2011; Draganski et al., 2004; Hanggi et al., 2010;
Jancke et al., 2009].
The cerebral neuroanatomical underpinnings of motor
skills have been studied in differently motor-expert indi-
viduals, ranging from highly trained professional musi-
cians [Hutchinson et al., 2003], to experienced typists
[Cannonieri et al., 2007], and basketball players [Park
et al., 2009]. These studies indicate that skill acquisition
and training in various domains, such as motor or cogni-
tive functions, evoke substantial changes in brain anatomy
and the increase of cerebellar volume represents one of the
main structural adaptation to long-term motor training.
The present study was aimed at exploring whether the
peculiar vertical movement characterizing the rock climb-
ing can induce cerebellar volume differences in world-
class mountain climbers (MC) compared to control group
(CG); and whether eventual cerebellar morphometry modi-
fications were associated to neocortical gray matter (GM)
volume in world-class MC.
For this purpose, we applied two different and well-vali-
dated structural analysis techniques: a region of interest (ROI)
imaging approach, based on manual tracing of the ROIs, to
investigate cerebellar volume changes; and the voxel-based
morphometry (VBM), an automatic images procedure, to ana-
lyze the whole brain GM and investigate whether cerebellar
volumes (ROIs) are related to neocortical GM.
MATERIAL AND METHODS
Subjects
A rare group of ten male world-class MC with previous
high-level experience of climbing in the Alps, Himalayas
and Andes, were included in this study (Table I).
All of them had been for at least 10 years before we col-
lected MRI images. MRI images of nine out of 10 world-
class MC have been already reported in a previous study
on gray and white matter cerebral changes [Di Paola et al.,
2008]. Ten healthy male subjects with similar age, anthro-
pometric traits and with no experience in climbing, were
selected as CG to cross-match comparisons (more details
in [Di Paola et al., 2008]). As shown in Table I, there were
no significant differences in demographic and anthropo-
metric data between groups. Before participating in the
study, all subjects (world-class MC and CG) read and
signed the informed consent form. All participants pro-
vided written informed consent. Consent was obtained
according to the Declaration of Helsinki, and the study
was approved by the ethical committee of IRCCS Santa
Lucia Foundation, Rome, Italy.
TABLE I. Demographic and anthropometric data
Word-class MC
(n¼10)
CG
(n¼10)
Student’s
T
P
value
Age (years SD) 38 (8) 39 (8) t
(18)
¼0.21 0.8
Gender All men All men
Handedness (The Edinburgh
Handedness Inventory)
All right-handed All right-handed
Height (cm SD) 176 (5) 175 (6) t
(18)
¼0.47 0.6
Weight (kg SD) 70.8 (6) 71.4 (6) t
(18)
¼0.35 0.7
BMI (kg/m
2
SD) 22.6 (1) 21.4 (4) t
(18)
¼0.94 0.4
World-class MC, world-class mountain climbers; CG, control group; BMI, body mass index.
rDi Paola et al. r
r2708 r
MRI Acquisition
All MRI data were acquired at IRCCS Santa Lucia Foun-
dation, Rome, Italy, by using an MR scanner operating at
1.5T (Siemens, Magnetom Vision, Erlangen, Germany). All
world-class MC were assessed 8 weeks after they returned
from the expedition [mean time in weeks (SD) ¼7.6 (0.7)].
The following pulse sequences, for both world-class MC
and CG, were obtained in a single session: (a) axial T2-
weighted fast spin-echo (SE) (TR/TE: 3800/90 ms); (b) axial
fluid-attenuated inversion-recovery (FLAIR) (TR/TE: 9.000/
119 ms; TI: 2.470 ms); (c) 3D T1-weighted magnetization-
prepared rapid-acquisition gradient echo (MPRAGE) (TR/
TE: 11.4/4.4 ms; TI: 20 ms; flip angle: 15). For the T2-
weighted and FLAIR sequences, 21 axial slices, 5-mm-thick,
with an intersection gap of 1 mm, a 240 mm field of view,
and a 256 256 matrix were acquired. For the MPRAGE
sequence, 159 slices, 1 mm-thick, with sagittal orientation, a
256256 matrix size, and a 256 mm field of view were
acquired. Two experienced observers (M.D.P. and U.S.),
unaware of whom the scans belonged to, independently
reviewed the T2-weighted and FLAIR scans of all subjects
to identify, by consensus, pathological hyperintensities.
MRI Analysis and Post-Processing
Radiofrequency bias field corrections were applied to all
images, to eliminate intensity drifts due to magnetic field inho-
mogeneities [Sled et al., 1998]. To adjust cerebral measurements
for individual and group differences in brain size, in order to
reduce the interindividual variability in gross brain size, differ-
ent reference measures such as forebrain volume, cranial
capacity, or cross-sectional cerebral area have been used in var-
ious studies either as a ratio [Jancke et al., 1997, 1999a], or as a
covariate corrected statistic [Schmitt et al., 2001a; Wang et al.,
1992]. Recently, by testing different methods [Bermudez and
Zatorre, 2001], it was concluded that a reliable brain volume
normalisation could be obtained by registering the MRI brain
volumes into the Talairach proportional stereotaxic space using
the algorithm developed by Collins et al. [1994]. In this way,
gross brain size differences are ruled out and the error-prone
collecting of an index of brain size is circumvented. For these
reasons, in this study, to adjust cerebral measurements for indi-
vidual and group differences in brain size, each of the MRI
brain volumes, from which the cerebellar measures were col-
lected, have been registered into the Talairach proportional ste-
reotaxic space using a nine-parameter registration algorithm
similar to that used in the previous study [Bermudez and
Zatorre, 2001]. The normalised Talairach stereotaxic space cere-
bellar measures were obtained by applying the appropriate
dimension of scaling recovered during the Talairach stereotaxic
brain volume transformation.
Cerebellar Vermis Volume
The cerebellar vermis was traced on the midsagittal slice.
The midsagittal slice was identified by selecting the sagittal
image showing lobular anatomy of the vermis, cerebral aque-
duct, corpus callosum, spinal cord, and fourth ventricle. The
boundaries were delineated according to the previously exist-
ing protocol [Mostofsky et al., 1998; Schmitt et al., 2001b].
Briefly, after the midsagittal MRI section was selected, the cer-
ebellar vermis was subdivided into three ROIs. The vermian
ROI1 (anterior vermis) including the lobules I–V, the vermian
ROI2 including the lobules VI and VII, and the vermian ROI3
(posterior vermis) including the lobules VIII–X. The cerebellar
tonsils and hemispheres were excluded from the vermian
ROIs (Fig. 1A). The whole protocol for segmentation of the
cerebellar vermis is described elsewhere [details in Mostofsky
et al., 1998; Schmitt et al., 2001b].
The significance level was adjusted for the 5 independ-
ent statistical comparisons (vermian lobules I-V; vermian
lobules VI-VII, vermian lobules VIII–X, left hemisphere
and right hemisphere, see paragraph below) (Bonferroni
correction, P¼0.05/5 0.01).
Cerebellar Hemisphere Volume
To trace each cerebellar hemisphere, the hemispheric
GM and white matter, the cerebellar tonsils, the vellum,
and the corpus medullare were taken into account,
whereas the vermis, the cerebellar peduncles, and the
fourth ventricle were excluded. The protocol for segmenta-
tion of the cerebellum hemisphere is described elsewhere
(details in [Park et al., 2006; Raz et al., 2001]) (Fig. 1B).
All cerebellar ROIs (vermian lobules and hemispheres) were
mapped by using DISPLAY, an interactive program developed
by J.D. McDonald (Montreal Neurological Institute). This pro-
gram permits the labelling of voxels belonging to an anatomi-
cal region on each section of the MRI brain volume and allows
for simultaneous visualization in 3D of the movement of the
cursor in the sagittal, axial, and coronal planes of the MRI. Any
volume can be selected by using the DISPLAY mouse-brush to
color the voxels of the volume in the ROI. This coloring proce-
dure accompanied by the 3D view of the MRI planes allows an
unambiguous identification of the ROI. The ROI was identified
by its landmarks and the voxels of this volume were then col-
ored. It is important to point out that DISPLAY extracts the
value of each MRI voxel intensity by positioning the cursor on
it and can also color code the images according to the pixel in-
tensity value. Accepted intrarater reliability for the volumetric
measures was Cohen j>0.80.
The significance level was adjusted for the five inde-
pendent statistical comparisons (vermian lobules I–V; ver-
mian lobules VI–VII, vermian lobules VIII–X, left
hemisphere and right hemisphere, see paragraph below)
(Bonferroni correction, P¼0.05/5 0.01).
Correlations Between Cerebellar Measure and
Whole-Brain GM Volume in World-Class MC
Group
We were interested in studying whether and how
differences in cerebellar morphometry (vermis and/or
rCerebellum Modifications in Expert Rock Climbers r
r2709 r
hemispheres) in world-class MC group were associated to
whole-brain GM volume modifications. Thus, we run a
multiple regression analysis in SPM5 (Wellcome Depart-
ment of Imaging Neuroscience, University College London,
UK), entering in the matrix the GM maps for each world-
class MC subject and the values of those cerebellar subre-
gions resulted different in our world-class MC group when
compared with CG, by the main analyses.
To obtain whole-brain GM maps, we processed and ana-
lyzed the images, by using VBM analysis [Ashburner and
Friston, 2000; Good et al., 2001] in the statistical parametric
mapping framework (SPM5, Wellcome Department of
Imaging Neuroscience, University College London, UK).
To improve image registration, images were first manually
reoriented to approximate the orientation to that of the
ICBM-152 default SPM5 template. Each volume was seg-
mented into GM partitions. Then, the Diffeomorphic Ana-
tomical Registration Through Exponential Lie Algebra
(DARTEL) toolbox was applied to the GM partitions. This
imaging processing allows a high-dimensional normaliza-
tion, better preserving brain topology. Template creation is
incorporated into the algorithm and a new template based
on the entire sample is created at the end of each iteration.
This technique improves the realignment of small inner
structures [Yassa and Stark, 2009]. Then, we used a script,
for transforming DARTEL template and images to MNI
space (D. MacLaren, pers. commun.). Finally, GM parti-
tions (modulated data) were smoothed using a Gaussian
kernel of 8 mm full width at half maximum (FWHM) and
entered into subsequent statistical analyses.
For each subject (world-class MC and CG) we extracted
and averaged the voxels of those cerebellar regions we
found different, as result of the main world-class MC vs.
CG morphometric analysis. Then we run two (one for
each group of subjects) correlational analyses in SPM5,
entering the total GM values as covariate. Given the lack
of literature data linking cerebellar and neocortical GM
features in rock climbers, we performed an exploratory
investigation, using an uncorrected threshold (to reduce
the risk of excluding false-negatives).
Statistical Analysis
All data were normally distributed (Shapiro–Wilk’s test)
and no significant difference in the distribution of variance
was present among dependent variables across subjects
(Levene’s Test). Data belonging to world-class MC and CG
were compared by applying Student’s t-test for independ-
ent groups. Furthermore, cerebellar measures and whole-
brain GM volumes in world-class MC group were corre-
lated by using a multiple regression in SPM5.
RESULTS
By correlating age of subjects and cerebellar volumes
(vermian lobules and hemispheres), no significant correla-
tion was found either in world-class MC and CG subjects.
The volumes of left and right hemispheres were highly
significantly correlated in both world-class MC (r¼0.941;
Figure 1.
Cerebellar regions of interest tracing. Panel Ashows the circum-
scription of the cerebellar vermis on the midsagittal brain slice (X
¼0). The vermis is divided into three portions, the lobules I–V
(in red), lobules VI–VII (in green), and lobules VIII–X (in blue).
Panel Bshows a representative image of a 3D model of the cere-
bellum. In light-blue cerebellar hemispheres, in fuchsia the whole
(3D) vermian lobules (although, in the present study we meas-
ured only the vermian midsagittal slice, as shown in Panel A).
rDi Paola et al. r
r2710 r
P<0.0001) and CG (r¼0.995; P<0.0001) groups. Con-
versely, total volumes of the hemispheres positively corre-
lated with volume of vermian lobules VIII-X only in CG
subjects (right hemisphere vs. lobules VIII–X, r¼0.784;
P¼0.007; left hemisphere vs. lobules VIII–X, r¼0.795;
P¼0.006). In fact, in world-class MC subjects such corre-
lations were not significant (right hemisphere vs. lobules
VIII–X, r¼0.055; P¼0.881; left hemisphere vs. lobules
VIII–X, r¼0.074; P¼0.839).
Cerebellar Vermis Volumes
World-class MC group had a larger total vermis volume
compared to CG as revealed by the Student’s t-test (t(18)
¼2.864; P¼0.01). Namely, lobules I–V contributed in
determining the significant difference in the cerebellar ver-
mis volume between groups. In fact, lobule I–V volume
was greater in world-class MC subjects compared with the
controls (t(18) ¼3.632; P¼0.002). Nevertheless, also the
other cerebellar lobules (VI–VII and VIII–X) presented
larger volumes in world-class MC compared with CG,
although differences did not reach the significance level
(Table II and Fig. 2).
Cerebellar Hemisphere Volumes
No significant difference in the cerebellar hemispheres
volumes between groups was found, as revealed by the
Student’s t-test, although once more the values of the
hemisphere volumes in world-class MC were bigger com-
pared with CG (Table II).
Correlations Between Cerebellar Measures and
Whole-Brain GM Volume in World-Class MC
Group
Given the main morphometric analysis showed that the
principal difference between world-class MC and CG was
at level of the lobules I–V, we extracted the mean value of
this cerebellar area for each world-class MC and CG sub-
ject. Then, we run two separate multiple regression analy-
ses in SPM5, by correlating lobules I–V values to the
whole GM map both in world-class MC and CG groups
separately (as we described previously).
Interestingly, a positive correlation between the lobules
I–V and the right medial posterior parietal area (superior
TABLE II. Cerebellar volumes
Subjects
Vermis Hemisphere
Whole Lobules I-V Lobules VI-VII Lobules VIII-X Left Right
Word-Class MC Mean (SD) 1.33 (0.09) 0.55 (0.04) 0.34 (0.03) 0.44 (0.05) 87.7 (6.3) 88.0 (5.2)
CG Mean (SD) 1.21 (0.10) 0.49 (0.03) 0.30 (0.06) 0.42 (0.06) 81.8 (12.1) 82.9 (12.5)
Student’s t-test t
(18)
2.864;
P¼0.01
3.632;
P¼0.002
1.710;
P¼0.104
0.991;
P¼0.335
1.364;
P¼0.19
1.212;
P¼0.241
Volumes are reported in cm
3
. World-class MC, world-class mountain climbers; CG, control group
Figure 2.
Vermian lobules overlapping. The vermian midsagittal slice vol-
ume (X¼0) of one world-class MC subject (in green) and one
CG subject (in red) are overlaid, after normalization, on the
rock climber T1-weighted normalized brain. In world-class MC,
the whole vermis appears bigger, but just lobules I–V are signifi-
cantly larger in comparison to CG. MC, world-class mountain
climber; CG, control group.
Figure 3.
Correlations between vermian lobules I–V and gray matter. The
significant positive correlations between the vermian midsagittal
slice volume of lobules I–V and neocortical GM map volume in
world-class MC group is illustrated. Results are shown at cluster
level P¼0.001 uncorrected. SPL, superior parietal lobule; R,
right.
rCerebellum Modifications in Expert Rock Climbers r
r2711 r
parietal lobules, SPL) (P¼0.001 uncorrected) was found
only in the world-class MC group (Fig. 3).
Moreover, there was no significant difference in average
whole cortical brain volume between world-class MC and
CG (mean SD, MC: 1,540 290 ml; CG: 1,529 220 ml,
P¼0.33, n.s.).
DISCUSSION
In the last decades, in vivo macrostructural brain change
associated to disease condition received a lot of interest. In
some cases the brain modification has been suggested to be
used as a biomarker [Dubois et al., 2007]. In pathologies, dif-
ferent pattern of increased/decreased brain volumes can be
related to distinct diseases or phenotypes [Baldacara et al.,
2011a,b; Bolduc et al., 2011; Cauda et al., 2012; Watson et al.,
2012]. In healthy subjects with specific excellent learned abil-
ities, usually increased volume in definite brain regions has
been reported [Gaser and Schlaug, 2003; Hutchinson et al.,
2003]. Even the lower metabolic activity described in the brain
regions involved in peculiar skills seems to reflect the minor
effort in executing the motor performance by the skilled group
compared to control group [Koeneke et al., 2004]. According
to these data we expected to find an increased cerebellum vol-
ume in our world-class MC. Indeed, in agreement with previ-
ous literature [Cannonieri et al., 2007; Hutchinson et al., 2003;
Park et al., 2009], the present findings demonstrate that long-
term motor training occurring in adulthood is associated to
cerebellar modifications not randomly distributed, but related
to the specific features of the motor skills. Namely, we found a
macrostructural difference in the volume of vermian lobules
I–V in world-class MC long practicing vertical movements,
compared to age/gender-matched controls with no experi-
ence in rock climbing.
Similar to other studies, analyzing the relations between
brain structure and function [Hutchinson et al., 2003], we
are unable to determine whether the structural differences
we observed exist as a result of differences in function
(prolonged and unusual motor experience) or whether the
structural difference enabled the difference in function to
arise. In other words, we are unable to determine whether
a climber brain will produce an expert climber or whether
an expert climber will modify his brain in a climber brain.
Interestingly, animal studies demonstrate that differences
in experiences and behaviors lead to structural differences
of the brain in general, and of the cerebellum in particular.
Animals whom environment requires to learn new motor
skills, as opposed to execute mere motor activity, present
an increase in size and numbers of synapses per Purkinje
cell, in the cerebellar cortex [Black et al., 1990]. Further-
more, animals reared in an enriched environment allowing
acquisition of complex motor behaviors, show increase in
density and length of dendritic spines along the distal
dendrites of Purkinje cells [Lee et al., 2007], differences in
spine density and dendritic branching of striatal interneur-
ons [Cutuli et al., 2011] and in pyramidal neocortical neu-
rons [Gelfo et al., 2009].
The observation of structural changes related to motor
skill acquisition fits particularly well with the well-known
cerebellar involvement in motor learning and adaptation
[Smith and Shadmehr, 2005; Criscimagna-Hemminger
et al., 2010]. Furthermore, the lack of macrostructural dif-
ferences in other vermian lobules, as well as in the hemi-
spheres, in world-class MC supports the notion that the
specific features of the motor skills are responsible for
plastic changes in the different anatomical areas [Hutchin-
son et al., 2003; Park et al., 2006; Park et al., 2009]. For
example, in basketball players, where the movement is
mainly linked to eye-hand coordination for dribbling, visu-
ally guided saccades and bimanual coordination for
‘‘shooting’’ the ball through the top of a basketball hoop,
Park et al. [2009] found an enlargement in different ver-
mian lobules, specifically in lobules VI–VII.
As shown by PET studies on movement control, most
cerebellar signals are attributable to sensory information
processing [Jueptner and Weiller, 1998]. And indeed the
cerebellum strongly utilizes kinesthetic feedback to moni-
tor and coordinate movements, thereby acting as a sen-
sori-motor predictor based on a combination of sensory
inputs and efference copies of motor commands [Bastian,
2006; Kleber et al., 2009]. Additionally, cerebellar function
is highly correlated with the timing of complex sequential
movements [Braitenberg et al., 1997; Doyon et al., 1997;
Mandolesi et al., 2010].
All these mentioned neuro-physiological features of cer-
ebellum account for its involvement in rock climbing activ-
ity, which requires accurate control of vertical quadruped
locomotion involving complex and unusual postural
adjustments, arm-leg coordination for the diagonal gait,
eye-hand coordination for reaching and grasping move-
ments and motor learning to maintain accurate movements
and balance in the presence of external or internal
perturbations.
Another interesting aspect of rock climbing is the pecu-
liar role of the upper limbs. Indeed, while at rest on a ver-
tical wall a hanging rock climber keeps his balance due to
horizontal supporting forces, when he releases one hold,
the vertical and horizontal forces, no more equally distrib-
uted on the remaining holds, counteract the perturbations
and balance the climber on the remaining holds. Thus,
rock climbing is characterised by sustained and intermit-
tent bouts of isometric forearm contractions, with, as con-
sequence, an increased demand placed upon the upper
body during climbing. Thus, climbers exhibit greater
strength and endurance in the fingers, arms, and should-
ers. Accordingly to this, world-class MC group exhibited a
significant enlargement of the vermian lobules I–V, which
are involved in dexterous finger and hand movements
[Catalan et al., 1998; Sadato et al., 1996], especially under
high demands of hand movement [Debaere et al., 2004;
Jancke et al., 1999b], as well as in eye-hand coordination
in the detection of and correction for visuomotor errors.
These data are also in agreement with the functional to-
pography of the cerebellum [Manni and Petrosini, 2004;
rDi Paola et al. r
r2712 r
Schmahmann, 1991, 1996, 2004; Stoodley and Schmahmann,
2010] in which cerebral cortical areas concerned with senso-
rimotor processing are linked with the cerebellar anterior
lobe (lobules I–V). In particular, movement of the hand
localizes to ipsilateral lobules V (and VIII) [Grodd et al.,
2001] and leg and foot sensorimotor representations are
observed in lobules II and III. Even the cerebellar motor
syndrome, characterized by impairment of balance and gait
ataxia, limb dysmetria, and oculomotor disorders, results
when lesions involve the anterior lobe (lobules I–V) and
parts of lobule VI, interrupting thus cerebellar communica-
tion with cerebral and spinal motor systems.
We have also found that in our world-class MC group
the enlargement of lobules I–V was related to the enlarge-
ment of right medial posterior parietal area (superior pari-
etal lobules, SPL). The parietal cortex receives input from
the cerebellum via the thalamus [Clower et al., 2001] and
sends connections in the opposite direction via the pons
[Glickstein, 2000]. The right medial posterior parietal area
(superior parietal lobules, SPL) is part of a circuit involved
in hand orientation during reaching and grasping move-
ments. Thus, it serves in locating objects in space and
serves as a point of convergence between vision and pro-
prioception to determine where objects are in relation to a
spatial reference frame [Fattori et al., 2009; Filimon, 2010].
Since both the parietal lobe and the cerebellum play a role
in sensorimotor prediction [Blakemore and Sirigu, 2003], it
is likely that they work in parallel to predict the sensory
consequences of movement, and to monitor and make
movement corrections. Clearly, action prediction is of
extreme importance during climbing and can make the
difference between survive or not at extreme altitude.
ACKNOWLEDGMENTS
Special thanks go to Drs. A. Zijdenbos, J.D. Mac- Donald
D.L. Collins and A.C. Evans of the Montreal Neurological
Institute, McGill University, Canada, for providing us with
software for image analysis.
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The cerebellum is involved in the learning and retention of motor skills. Using animal and human models, a number of studies have shown that long-term motor skill training induces structural and functional plasticity in the cerebellum. The aim of this study was to investigate whether macroscopic alteration in the volume of cerebellum occurs in basketball players who had learned complex motor skills and practiced them intensively for a long time. Three-dimensional magnetic resonance imaging volumetry was performed in basketball players (n = 19) and healthy controls (n = 20), and the volumes of cerebellum and vermian lobules were compared between two groups. Although there was no macroscopic plasticity detected in the cerebellum as a whole, detailed parcellation of cerebellum revealed morphological enlargement in the vermian lobules VI–VII (declive, folium, and tuber) of basketball players (P < 0.0166), which might then be interpreted as evidence for plasticity. This finding suggests that the extensive practice and performance of sports-related motor skills activate structural plasticity of vermian lobules in human cerebellum and suggests that vermian VI–VII plays an important role in motor learning.
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At its simplest, voxel-based morphometry (VBM) involves a voxel-wise comparison of the local concentration of gray matter between two groups of subjects. The procedure is relatively straightforward and involves spatially normalizing high-resolution images from all the subjects in the study into the same stereotactic space. This is followed by segmenting the gray matter from the spatially normalized images and smoothing the gray-matter segments. Voxel-wise parametric statistical tests which compare the smoothed gray-matter images from the two groups are performed. Corrections for multiple comparisons are made using the theory of Gaussian random fields. This paper describes the steps involved in VBM, with particular emphasis on segmenting gray matter from MR images with nonuniformity artifact. We provide evaluations of the assumptions that underpin the method, including the accuracy of the segmentation and the assumptions made about the statistical distribution of the data.
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Voxel-based-morphometry (VBM) is a whole-brain, unbiased technique for characterizing regional cerebral volume and tissue concentration differences in structural magnetic resonance images. We describe an optimized method of VBM to examine the effects of age on grey and white matter and CSF in 465 normal adults. Global grey matter volume decreased linearly with age, with a significantly steeper decline in males. Local areas of accelerated loss were observed bilaterally in the insula, superior parietal gyri, central sulci, and cingulate sulci. Areas exhibiting little or no age effect (relative preservation) were noted in the amygdala, hippocampi, and entorhinal cortex. Global white matter did not decline with age, but local areas of relative accelerated loss and preservation were seen. There was no interaction of age with sex for regionally specific effects. These results corroborate previous reports and indicate that VBM is a useful technique for studying structural brain correlates of ageing through life in humans.