Research in Developmental Disabilities 35 (2014) 2352–2358

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Visuomotor processing and hand force coordination in

dyslexic children during a visually guided manipulation task
Paulo B. de Freitas a,*, Sabrina T. Pedão a, Jose A. Barela a,b
a
Graduate Program in Human Movement Science, Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, São Paulo,
SP, Brazil
b
Department of Physical Education, Institute of Biosciences, São Paulo State University, Rio Claro, SP, Brazil

A R T I C L E I N F O A B S T R A C T

Article history: Developmental Dyslexia negatively affects children’s reading and writing ability and, in most
Received 3 May 2014 cases, performance in sensorimotor tasks. These deficits have been associated with
Accepted 3 June 2014 structural and functional alterations in the cerebellum and the posterior parietal cortex
Available online 22 June 2014 (PPC). Both neural structures are active during visually guided force control and in the
coordination of load force (LF) and grip force (GF) during manipulation tasks. Surprisingly,
Keywords: both phenomena have not been investigated in dyslexic children. Therefore, the aim of this
Dyslexia study was to compare dyslexic and non-dyslexic children regarding their visuomotor
Grip
processing ability and GF–LF coordination during a static manipulation task. Thirteen
Load
dyslexic (8–14 YO) and 13 age- and sex-matched non-dyslexic (control) children
Coupling
Reading problem
participated in the study. They were asked to grasp a fixed instrumented handle using
Feedback the tip of all digits and pull the handle upward exerting isometric force to match a ramp-and-
Control hold force profile displayed in a computer monitor. Task performance (i.e., visuomotor
coordination) was assessed by RMSE calculated in both ramp and hold phases. GF–LF
coordination was assessed by the ratio between GF and LF (GF/LF) calculated at both phases
and the maximum value of a cross-correlation function (rmax) and its respective time lag
calculated at ramp phase. The results revealed that the RMSE at both phases was larger in
dyslexic than in control children. However, we found that GF/LF, rmax, and time lags were
similar between groups. Those findings indicate that dyslexic children have a mild deficit in
visuomotor processing but preserved GF–LF coordination. Altogether, these findings
suggested that dyslexic children could present mild structural and functional alterations in
specific PPC or cerebellum areas that are directly related to visuomotor processing.
ß 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Developmental dyslexia is a common neurological condition affecting children’s reading and writing performance,
averting them to achieve the expected ability for a particular age (Brookes, Tinkler, Nicolson, & Fawcett, 2010; Nicolson,
Fawcett, & Dean, 2001). Despite that, children with dyslexia have normal and even above normal intelligence level.
Therefore, these problems could not be accounted for lack of sufficient educational opportunities. Besides having reading and
writing deficits, most dyslexic children have poor performance in tests involving sensorimotor integration. For instance, the

* Corresponding author at: Instituto de Ciências da Atividade Fı́sica e Esportes – ICAFE, Universidade Cruzeiro do Sul, Rua Galvão Bueno, 868, São Paulo,
SP 01506-000, Brazil. Tel.: +55 11 3385 3103.
E-mail addresses: deFreitasPB@gmail.com, Paulo.deFreitas@cruzeirodosul.edu.br (P.B. de Freitas).

http://dx.doi.org/10.1016/j.ridd.2014.06.002
0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358 2353

findings of several studies have shown that dyslexic children manifest poor performance during task requiring control of
body posture (Barela, Dias, Godoi, Viana, & de Freitas, 2011; Brookes et al., 2010; Moe-Nilssen, Helbostad, Talcott, &
Toennessen, 2003; Stoodley, Fawcett, Nicolson, & Stein, 2005; Viana, Razuk, de Freitas, & Barela, 2013) and gait (Moe-Nilssen
et al., 2003). Moreover, dyslexic children showed decreased performance in tasks involving manual skills (Fawcett &
Nicolson, 1995; Leslie, Davidson, & Batey, 1985).
Based upon the evidences that dyslexic children have sensorimotor deficits, it has been suggested that dyslexia could have a
cerebellar cause (Nicolson et al., 2001; Nicolson, Daum, Schugens, Fawcett, & Schulz, 2002). This suggestion has been supported
by findings of neuroimage and anatomical studies (Eckert et al., 2003; Finch, Nicolson, & Fawcett, 2002; Laycock et al., 2008; Rae
et al., 2002), which showed that dyslexic individuals have structural cerebellar differences when compared to non-dyslexic
peers. However, other studies have shown that structural neural changes in dyslexic individuals are not only restricted to the
cerebellum, but affects several brain regions (Brown et al., 2001; Galaburda & Livingstone, 1993; Green et al., 1999; Pennington,
1999). For example, individuals with dyslexia present structural changes in the magnocellular pathway that affect posterior
parietal cortex (PPC) function (Facoetti & Molteni, 2001; Galaburda & Livingstone, 1993; Stein & Walsh, 1997).
It is already known that both, PPC and cerebellum, have a crucial role in visuomotor processing during tasks that requires
steadiness in isometric force exertion guided by visual feedback (Vaillancourt, Thulborn, & Corcos, 2003; Vaillancourt,
Mayka, & Corcos, 2006) as well as in the control of manipulation tasks (Babin-Ratte, Sirigu, Gilles, & Wing, 1999; Boecker
et al., 2005; Ehrsson, Fagergren, Johansson, & Forssberg, 2003; Kawato et al., 2003; Nowak, Hermsdorfer, Marquardt, & Fuchs,
2002). Surprisingly, as far as we know no available research exists investigating visuomotor processing during isometric
force exertion and hand forces coordination in dyslexic children.
An elegant experimental paradigm has been employed to investigate the relationship between force components acting
on the digits and object surface interaction during several object manipulation tasks. The force component acting
tangentially on the digits–object interaction, referred to as load force (LF), tends to cause slippage of the hand-held object,
which is prevented by the exertion of force perpendicularly against the object surface, which has been termed grip force (GF)
(Johansson & Westling, 1984; Westling & Johansson, 1984). The close relationship established between GF and LF during
object manipulation is a striking evidence of the central nervous system’s (CNS) ability to predict the effects of individuals
own actions and the cerebellum is the neural structure responsible for this prediction (Blakemore, Goodbody, & Wolpert,
1998; Flanagan & Wing, 1995). In addition, the results of neuroimage studies have also shown the participation of PPC areas
in GF–LF coordination (Boecker et al., 2005; Ehrsson et al., 2003).
GF–LF coordination has been investigated during manipulation tasks that involve lifting a grasped object (Johansson &
Westling, 1984), moving a handheld object upward and downward discretely (Flanagan & Wing, 1993) or continuously
(Flanagan & Wing, 1995; Zatsiorsky, Gao, & Latash, 2005), and isometrically applying sinusoidal LF profiles on an externally
fixed object (Blakemore et al., 1998; de Freitas & Jaric, 2009; Jaric, Collins, Marwaha, & Russell, 2006). The use of an externally
fixed object to perform manipulation tasks could bring additional information about the individual’s ability to control LF (i.e.,
task performance) over the task time course (Pedao, Barela, Lima, & de Freitas, 2013). Specifically, in addition to evaluate GF–
LF coordination we could assess visuomotor processing during this task by asking the participants to exert a certain amount
of force in order to match or superpose a force profile (i.e., force line target) shown in a computer monitor. Therefore, the
aims of this study were to examine the visuomotor processing and the GF–LF coordination of dyslexic children during a
manipulation task performed in an externally fixed handle with visual feedback of the exerted LF presented in real time and
to compare them with normal reader children. We hypothesized that both GF–LF coordination and task performance (i.e.,
visuomotor coordination) would be affected in dyslexic children, with them showing poorer indices of GF–LF coordination
and task performance than normal reader children.

2. Methods

2.1. Participants

Thirteen dyslexic children aging between 9 and 14 years-old (mean  SD, 11.3  1.8 year-old) and 13 age and gender-
matched children (11.4  2 year-old) participated of the study. Dyslexic children were diagnosed as mildly dyslexic by the
Brazilian Dyslexic Association (ABD) or CEFAC Institute both located in São Paulo, Brazil and recruited from both institutions.
Children from the control group were recruited from regular schools in São Paulo city and were classified as normal readers by
their teachers. All children were right-handed and handedness was determined by the Edinburgh Handedness Inventory
(Oldfield, 1971). The participation in the study was conditioned to the permission given by the parents and legal guardians by the
signature of an informed consent form approved by the University Institutional Ethics committee and follow the Declaration of
Helsinki.

2.2. Experimental apparatus

The instrumented handle used in the study is schematically depicted in Fig. 1. It is formed by two parallel aluminum
plates (15 cm  4 cm  1 cm) connected with each other by a load force (LPM-530, Cooper Instruments and Systems, USA)
and two aluminum pieces with a force and torque (F/T) transducer (Mini40, ATI, USA) in between them, forming the basis of
the handle. The opposing handle grasping surfaces were 5 cm apart and were covered with extra fine sandpaper (320 grit).
2354 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358

Fig. 1. Schematic representation of the experimental setup. The force profile and the vertical force (FZ) exerted by a child is highlighted on the right side of
the figure as well as the instrumented handle and the all force components recorded from the single-axis load cell and F/T transducer.

The compression force (FC) produced by the thumb against the instrumented object surface was obtained by the load cell
placed in between the aluminum plates, while information about all three force and torque components applied against the
handle by the tip of all digits was provided by the F/T transducer.

2.3. Experimental procedure

Before starting the experiment, the participant cleaned the tip of their digits with alcohol swab to remove all residues that
could affect the friction between the skin and the handle surface. Then, him/her stood upright, kept his/her upper arm
vertically and forearm horizontally oriented, and was asked to grasp the fixed handle using the tip of the digits as
represented in Fig. 1. The vertically oriented handle was rotated 458 with respect to the children’s frontal plane to afford a
comfortable wrist position. Next, the participants were requested to isometrically pull the instrumented handle up in order
to match (i.e., superpose) a prescribed force profile (target) that was composed of a constant zero force line lasting 2.5 s,
followed by a ascendant diagonal line (i.e., ramp) lasting also 2.5 s, and a constant 5 N force line (i.e., constant) lasting 7 s
(Fig. 1). The force target and the current real-time vertical force (FZ) exerted by the participants were displayed in a 19-in.
widescreen computer monitor placed in front of them. While the target was showed as a continuous red line, the FZ was
shown as a continuous left to right running black line in a white background. Each trial lasted 12 s. Participants performed
two blocks of three trials to familiarize with the task, which ensured adequate task performance, followed by three trials that
were recorded and analyzed.

2.4. Data processing and analyses

For data acquisition and processing, we used two customized LabView (National Instruments, USA) routines. The force
signals were recorded at 200 Hz and stored for future analyses. The raw force signals were low-pass filtered with a 4th-order,
zero lag, Butterworth filter with a cut-off frequency set at 20 Hz. Following, GF and LF were calculated. The LF was calculated
as the resultant force of the two tangential force components (i.e., vertical FZ and horizontal FX, LF = HFZ2 + FX2) and GF was
calculated by averaging the force exerted against two sides of the handle (i.e., FC recorded by the load cell and FY recorded by
the F/T transducer) (de Freitas, Uygur, & Jaric, 2009; Uygur, de Freitas, & Jaric, 2010; Uygur, Prebeg, & Jaric, 2014). Regarding
the analysis of the ramp phase, although this phase lasted 2.5 s, only the interval between 0.25 and 2.25 s was analyzed since
we were not interested in the transitions related to the beginning and end of the ramp phase. Similarly, for the constant force
phase we skipped the first and the last second of the data.
To evaluate task performance (i.e., visuomotor coordination) during both ramp and constant phases we calculated the
root mean square error (RMSE) of the exerted FZ with respect to the target force. In addition, GF control was assessed by GF to
LF ratio (GF/LF) also in both phases, and the GF–LF coupling during the ramp phase was assessed by maximum value of a
cross-correlation function (rmax) and its respective time lag.
 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358 2355

2.5. Statistical analyses

After assuring that the data had normal distribution, we performed two one-way multivariate analyses of variance
(MANOVAs) and a single one-way analysis of variance (ANOVA). The first MANOVA was used to test the effect of group on
RMSE calculated during ramp and constant phases and the second MANOVA was used to test the effect of group on GF/LF also
during ramp and constant FZ exertion phases. When MANOVA reached significance, univariate analyses were performed.
Finally, the single one-way ANOVA was used to test the effect of group on the Fisher Z transformed rmax values. For all
performed analysis, the alpha value was set at .05.

3. Results

The results showed that all children after two blocks of practice were able to accomplish the task, matching both the ramp
phase and constant force phase with relative success. Fig. 2A depicts the averaged RMSE for each group in both phases: ramp
(left panel) and constant (right panel). Regarding group comparison, the MANOVA for RMSE indicated an effect of group
[Wilks’ Lambda = .671, F(2,23) = 5.627, p < .05]. Univariate analyses revealed that dyslexic children were less accurate (i.e.,
showed higher RMSE) than controls in both phases: ramp [F(1,24) = 10.54, p < .005, h2 = .31] and constant [F(1,24) = 5.74,
p < .05, h2 = .19].
Fig. 2B depicts the averaged GF/LF for each group in both phases: ramp and constant. MANOVA revealed no effect of group
[Wilks’ Lambda = .149, F(2,23) = 0.86, p > .05] on GF/LF. In addition, one-way ANOVA revealed no effect of group on the Fisher
Z transformed rmax values [F(1,24) = 3.34, p = .08, h2 = .12]. Both groups presented a very high directional GF–LF coupling
(median rmax equal to 0.973 and 0.984 for dyslexic and non-dyslexic children, respectively) and GF–LF time-lags were
virtually zero.

4. Discussion

The aims of the study were to examine the visuomotor processing and the GF–LF coordination of dyslexic children during
a manipulation task performed in an externally fixed handle with visual feedback of the exerted LF presented in real time and
compare them with normal reader children. The results revealed that the RMSE in both ramp and constant force phases was
larger in dyslexic when compared with non-dyslexic children, indicating that dyslexic children show a deficit in visuomotor
processing. However, we found that GF–LF coordination is similar between groups as shown by the lack of differences in GF/
LF, rmax, and time-lag.

Fig. 2. Bars represent averaged across subject values of (A) root mean square error (RMSE, in N) and (B) grip force to load force ratio (GF/LF) for each group,
dyslexic and control, and for each phase, ramp and constant. Error bars represent standard deviations.
2356 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358

The RMSE is a variable that describe the individual’s task performance, namely, the ability to exert a specific amount of
force in order to superpose a visual target displayed on a computer monitor. To perform this task, visual information about
the target and the force the person is exerting should be used by the CNS to plan the next step, keeping the rate of force
increase (in case of the ramp) or keeping force magnitude (in case of the constant phase) unchanged. The success in this task
depends on how the individuals use incoming visual information and transform them in ongoing motor commands. The high
RMSE in dyslexics indicates that these children have problems in visuomotor processing related to force production. It
happened when they needed to increase force in a constant pace during ramp phase and when they needed to maintain the
same force magnitude. Seemingly, this is the first study investigating dyslexic children performing this kind of task.
Our finding corroborates the results from other studies that showed that dyslexic children have problems with
sensorimotor coordination. Several studies have indicated that dyslexic children show poor performance in motor tasks such
as posture (Barela et al., 2011; Kapoula & Bucci, 2007; Moe-Nilssen et al., 2003) and gait (Moe-Nilssen et al., 2003) and our
results allow us to add that dyslexic children also show impaired visuomotor processing (i.e., higher RMSE) in a manipulation
task performed with visual feedback. Interestingly, the use of visual cues to control motor actions, such as upright stance in
conditions in which visual cues induce coherent sway, also is characterized by more variable and less coherent sway in
dyslexic children (Barela et al., 2011; Viana et al., 2013), which is in accordance with our findings. In addition, impaired
binocular coordination and, particularly, poor vergence abilities seems to account for some of the postural performance
deficit in dyslexic children (Kapoula & Bucci, 2007) and could also be the reason for a poorer performance in this visually
guided manipulation task. Taken all together these results, there are clear evidences that dyslexic children are capable of
performing sensorimotor tasks, however, not as precisely as normal reader peers.
Besides corroborating previous findings, our results shed light into some of the possible neurobehavioral changes in
dyslexic children. During visually guided isometric grip force control using visual feedback many cortical and subcortical
brain structures are involved. For example, Vaillancourt et al. (2003) using fMRI observed that parietal, premotor and
anterior prefrontal cortices, as well as supplementary motor area, putamen, ventral thalamus and cerebellum (lateral part
and dentate nucleus) are active during this kind of task. Because dyslexic children perform worse in this visuomotor task, it
might be suggested that they might have structural and functional changes in one or even more of these interconnected
brain structures. Possible candidates are the lateral cerebellum, the dentate nucleus as well as the PPC. Cerebellar
dysfunction has been associated to many of the dyslexic children’s poor performance in several tasks (e.g., Nicolson &
Fawcett, 2005; Nicolson et al., 2001) and has motivated much of the debate regarding the etiology of dyslexia (e.g., Irannejad
& Savage, 2012; Stoodley & Stein, 2011). Regarding the PPC, it is long known that this area is responsible for several functions
that are suggested to be impaired in dyslexic children, such as spatial localization and orientation of objects (e.g., a visual
target) and visuomotor coordination (Stein & Walsh, 1997). Going beyond the speculation about the causes of the dyslexia,
what is important regarding the poorer performance of dyslexic children in a visually guided force control task is that this
test is very simple to be applied and is able to distinguish dyslexic from non-dyslexic children and could be used to
discriminate children who could possibly have dyslexia as an auxiliary diagnosis tool.
Despite having poorer task performance, dyslexic children are able to properly scale GF to the task demand as non-
dyslexic children during both phases of the proposed manipulation task. Also, dyslexics are as able as non-dyslexic children
to change GF in parallel with changes in LF and change it with no time delay. A proper GF–LF coupling depends on the CNS’s
ability to predict own actions and, as previously mentioned, the cerebellum, and specifically its posterior part ipsilateral to
the hand used to perform the task (Boecker et al., 2005), is the neural structure involved in achieving such outcome
(Blakemore et al., 1998; Boecker et al., 2005; Flanagan & Wing, 1997; Kawato et al., 2003). In addition, GF–LF coupling during
isometric LF force exertion has also been associated with ipsilateral (right) activation of the PPC, specifically, with the
posterior intraparietal sulcus. Therefore, it seems that this area has an important role in manipulation task in which LF is
dynamically changed (Ehrsson et al., 2003). If dyslexic children have no changes in GF–LF coordination, someone could claim
that the function of both cerebellum and PPC is not affected by dyslexia. However, we also found that dyslexic children
present visuomotor processing deficits that are associated with impaired function of the same encephalic regions. Taken
together, the findings of this study indicate that dyslexia does not affect the whole cerebellum as well as the whole PPC.
There are specific areas within both, cerebellum and PPC that have their function affected by the dyslexia, while other areas
preserve their typical function.
Due to the importance of this research topic, new experiments should be performed. It seems certain that dyslexic
children have poorer visuomotor task performance, since the difference in performance between dyslexic and non-dyslexic
children was found even in a very simple task, that is, in a task that requires constant force exertion. However, we
recommend the use of manipulation tasks that impose continuous (cyclical) changes in LF in both fixed and free-moving
handles, which is considered more complex and challenging than the one in this study to confirm or even refute the
occurrence of changes in directional and, also, temporal coupling between GF and LF in dyslexic children.

5. Conclusion

The results of the present study indicate that dyslexic children have poorer performance in a task involving isometric
force production and control guided by visual feedback than normal reader children and it could be a sign that dyslexic
children present deficits in visuomotor processing that could be related to structural and functional alterations in either
specific PPC areas, or in specific parts of the cerebellum or both that are responsible for this processing. In addition, dyslexic
 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358 2357

children presented comparable GF–LF coordination than non-dyslexic children in this specific manipulation task, meaning
that they are able to properly scale GF with LF and predict the consequences of the change in LF during the ramp phase
changing GF in parallel and with no time delay with LF. As GF–LF coordination is also associated with some specific PPC and
cerebellum areas, we could suggest that those areas are not affected by dyslexia.

Acknowledgements

We thank the children and their parents who gave their time and effort to participate in this study. We also thank São
Paulo State Research Foundation (FAPESP, Brazil) for providing financial support to this research (#2010/02939-4 and
#2012/16365-5).

References

Babin-Ratte, S., Sirigu, A., Gilles, M., & Wing, A. (1999). Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration. Experimental Brain
Research, 128(1/2), 81–85.
Barela, J. A., Dias, J. L., Godoi, D., Viana, A. R., & de Freitas, P. B. (2011). Postural control and automaticity in dyslexic children: The relationship between visual
information and body sway. Research in Developmental Disabilities, 32(5), 1814–1821.
Blakemore, S. J., Goodbody, S. J., & Wolpert, D. M. (1998). Predicting the consequences of our own actions: The role of sensorimotor context estimation. Journal of
Neuroscience, 18(18), 7511–7518.
Boecker, H., Lee, A., Muhlau, M., Ceballos-Baumann, A., Ritzl, A., Spilker, M. E., et al. (2005). Force level independent representations of predictive grip force-load
force coupling: A PET activation study. Neuroimage, 25(1), 243–252.
Brookes, R. L., Tinkler, S., Nicolson, R. I., & Fawcett, A. J. (2010). Striking the right balance: Motor difficulties in children and adults with dyslexia. Dyslexia, 16(4),
358–373.
Brown, W. E., Eliez, S., Menon, V., Rumsey, J. M., White, C. D., & Reiss, A. L. (2001). Preliminary evidence of widespread morphological variations of the brain in
dyslexia. Neurology, 56(6), 781–783.
de Freitas, P. B., & Jaric, S. (2009). Force coordination in static manipulation tasks performed using standard and non-standard grasping techniques. Experimental
Brain Research, 194(4), 605–618.
de Freitas, P. B., Uygur, M., & Jaric, S. (2009). Grip force adaptation in manipulation activities performed under different coating and grasping conditions.
Neuroscience Letters, 457(1), 16–20.
Eckert, M. A., Leonard, C. M., Richards, T. L., Aylward, E. H., Thomson, J., & Berninger, V. W. (2003). Anatomical correlates of dyslexia: Frontal and cerebellar findings.
Brain, 126(Pt 2), 482–494.
Ehrsson, H. H., Fagergren, A., Johansson, R. S., & Forssberg, H. (2003). Evidence for the involvement of the posterior parietal cortex in coordination of fingertip
forces for grasp stability in manipulation. Journal of Neurophysiology, 90(5), 2978–2986.
Facoetti, A., & Molteni, M. (2001). The gradient of visual attention in developmental dyslexia. Neuropsychologia, 39(4), 352–357.
Fawcett, A. J., & Nicolson, R. I. (1995). Persistent deficits in motor skill of children with dyslexia. Journal of Motor Behavior, 27, 235–241.
Finch, A. J., Nicolson, R. I., & Fawcett, A. J. (2002). Evidence for a neuroanatomical difference within the olivo-cerebellar pathway of adults with dyslexia. Cortex,
38(4), 529–539.
Flanagan, J. R., & Wing, A. M. (1993). Modulation of grip force with load force during point-to-point arm movements. Experimental Brain Research, 95(1), 131–143.
Flanagan, J. R., & Wing, A. M. (1995). The stability of precision grip forces during cyclic arm movements with a hand-held load. Experimental Brain Research, 105(3),
455–464.
Flanagan, J. R., & Wing, A. M. (1997). The role of internal models in motion planning and control: Evidence from grip force adjustments during movements of hand-
held loads. Journal of Neuroscience, 17(4), 1519–1528.
Galaburda, A., & Livingstone, M. (1993). Evidence for a magnocellular defect in developmental dyslexia. Annals of the New York Academy of Sciences, 682, 70–82.
Green, R. L., Hutsler, J. J., Loftus, W. C., Tramo, M. J., Thomas, C. E., Silberfarb, A. W., et al. (1999). The caudal infrasylvian surface in dyslexia: Novel magnetic
resonance imaging-based findings. Neurology, 53(5), 974–981.
Irannejad, S., & Savage, R. (2012). Is a cerebellar deficit the underlying cause of reading disabilities? Annals of Dyslexia, 62(1), 22–52.
Jaric, S., Collins, J. J., Marwaha, R., & Russell, E. (2006). Interlimb and within limb force coordination in static bimanual manipulation task. Experimental Brain
Research, 168(1/2), 88–97.
Johansson, R. S., & Westling, G. (1984). Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or
more slippery objects. Experimental Brain Research, 56(3), 550–564.
Kapoula, Z., & Bucci, M. P. (2007). Postural control in dyslexic and non-dyslexic children. Journal of Neurology, 254(9), 1174–1183.
Kawato, M., Kuroda, T., Imamizu, H., Nakano, E., Miyauchi, S., & Yoshioka, T. (2003). Internal forward models in the cerebellum: fMRI study on grip force and load
force coupling. Progress in Brain Research, 142, 171–188.
Laycock, S. K., Wilkinson, I. D., Wallis, L. I., Darwent, G., Wonders, S. H., Fawcett, A. J., et al. (2008). Cerebellar volume and cerebellar metabolic characteristics in
adults with dyslexia. Annals of the New York Academy of Sciences, 1145, 222–236.
Leslie, S. C., Davidson, R. J., & Batey, O. B. (1985). Purdue pegboard performance of disabled and normal readers: Unimanual versus bimanual differences. Brain and
Language, 24(2), 359–369.
Moe-Nilssen, R., Helbostad, J. L., Talcott, J. B., & Toennessen, F. E. (2003). Balance and gait in children with dyslexia. Experimental Brain Research, 150(2), 237–244.
Nicolson, R. I., & Fawcett, A. J. (2005). Developmental dyslexia, learning and the cerebellum. Journal of Neural Transmission: Supplement, 69, 19–36.
Nicolson, R. I., Fawcett, A. J., & Dean, P. (2001). Developmental dyslexia: The cerebellar deficit hypothesis. Trends in Neuroscience, 24(9), 508–511.
Nicolson, R. I., Daum, I., Schugens, M. M., Fawcett, A. J., & Schulz, A. (2002). Eyeblink conditioning indicates cerebellar abnormality in dyslexia. Experimental Brain
Research, 143(1), 42–50.
Nowak, D. A., Hermsdorfer, J., Marquardt, C., & Fuchs, H. H. (2002). Grip and load force coupling during discrete vertical arm movements with a grasped object in
cerebellar atrophy. Experimental Brain Research, 145(1), 28–39.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.
Pedao, S. T., Barela, J. A., Lima, K. C., & de Freitas, P. B. (2013). Grip and load force coordination in cyclical isometric manipulation task is not affected by the feedback
type. Journal of Neuroengineering and Rehabilitation, 10, 34.
Pennington, B. F. (1999). Toward an integrated understanding of dyslexia: Genetic, neurological, and cognitive mechanisms. Development and Psychopathology,
11(3), 629–654.
Rae, C., Harasty, J. A., Dzendrowskyj, T. E., Talcott, J. B., Simpson, J. M., Blamire, A. M., et al. (2002). Cerebellar morphology in developmental dyslexia.
Neuropsychologia, 40(8), 1285–1292.
Stein, J., & Walsh, V. (1997). To see but not to read; the magnocellular theory of dyslexia. Trends in Neuroscience, 20(4), 147–152.
Stoodley, C. J., & Stein, J. F. (2011). The cerebellum and dyslexia. Cortex, 47(1), 101–116.
Stoodley, C. J., Fawcett, A. J., Nicolson, R. I., & Stein, J. F. (2005). Impaired balancing ability in dyslexic children. Experimental Brain Research, 167(3), 370–380.
Uygur, M., de Freitas, P. B., & Jaric, S. (2010). Frictional properties of different hand skin areas and grasping techniques. Ergonomics, 53(6), 812–817.
2358 P.B. de Freitas et al. / Research in Developmental Disabilities 35 (2014) 2352–2358

Uygur, M., Prebeg, G., & Jaric, S. (2014). Force control in manipulation tasks: Comparison of two common methods of grip force calculation. Motor Control, 18(1),
18–28.
Vaillancourt, D. E., Thulborn, K. R., & Corcos, D. M. (2003). Neural basis for the processes that underlie visually guided and internally guided force control in
humans. Journal of Neurophysiology, 90(5), 3330–3340.
Vaillancourt, D. E., Mayka, M. A., & Corcos, D. M. (2006). Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex.
Journal of Neurophysiology, 95(2), 922–931.
Viana, A. R., Razuk, M., de Freitas, P. B., & Barela, J. A. (2013). Sensorimotor integration in dyslexic children under different sensory stimulations. PLoS ONE, 8(8),
e72719.
Westling, G., & Johansson, R. S. (1984). Factors influencing the force control during precision grip. Experimental Brain Research, 53(2), 277–284.
Zatsiorsky, V. M., Gao, F., & Latash, M. L. (2005). Motor control goes beyond physics: Differential effects of gravity and inertia on finger forces during manipulation
of hand-held objects. Experimental Brain Research, 162(3), 300–308.