Research in Developmental Disabilities 35 (2014) 2352–2358
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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. Peda˜o a, Jose A. Barela a,b a Graduate Program in Human Movement Science, Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, Sa˜o Paulo, SP, Brazil b Department of Physical Education, Institute of Biosciences, Sa˜o 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: Received 3 May 2014 Accepted 3 June 2014 Available online
Developmental Dyslexia negatively affects children’s reading and writing ability and, in most cases, performance in sensorimotor tasks. These deficits have been associated with structural and functional alterations in the cerebellum and the posterior parietal cortex (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, both phenomena have not been investigated in dyslexic children. Therefore, the aim of this study was to compare dyslexic and non-dyslexic children regarding their visuomotor processing ability and GF–LF coordination during a static manipulation task. Thirteen dyslexic (8–14 YO) and 13 age- and sex-matched non-dyslexic (control) children participated in the study. They were asked to grasp a fixed instrumented handle using the tip of all digits and pull the handle upward exerting isometric force to match a ramp-andhold 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.
Keywords: Dyslexia Grip Load Coupling Reading problem Feedback Control
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 Cieˆncias da Atividade Fı´sica e Esportes – ICAFE, Universidade Cruzeiro do Sul, Rua Galva˜o Bueno, 868, Sa˜o Paulo, SP 01506-000, Brazil. Tel.: +55 11 3385 3103. E-mail addresses: [email protected], [email protected] (P.B. de Freitas). http://dx.doi.org/10.1016/j.ridd.2014.06.002 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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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 gendermatched 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 Sa˜o Paulo, Brazil and recruited from both institutions. Children from the control group were recruited from regular schools in Sa˜o 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).
[(Fig._1)TD$IG]
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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.
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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)TD$IG]
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.
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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 nondyslexic 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
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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 Sa˜o 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. 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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. Peda˜o a, Jose A. Barela a,b a Graduate Program in Human Movement Science, Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, Sa˜o Paulo, SP, Brazil b Department of Physical Education, Institute of Biosciences, Sa˜o 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: Received 3 May 2014 Accepted 3 June 2014 Available online
Developmental Dyslexia negatively affects children’s reading and writing ability and, in most cases, performance in sensorimotor tasks. These deficits have been associated with structural and functional alterations in the cerebellum and the posterior parietal cortex (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, both phenomena have not been investigated in dyslexic children. Therefore, the aim of this study was to compare dyslexic and non-dyslexic children regarding their visuomotor processing ability and GF–LF coordination during a static manipulation task. Thirteen dyslexic (8–14 YO) and 13 age- and sex-matched non-dyslexic (control) children participated in the study. They were asked to grasp a fixed instrumented handle using the tip of all digits and pull the handle upward exerting isometric force to match a ramp-andhold 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.
Keywords: Dyslexia Grip Load Coupling Reading problem Feedback Control
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 Cieˆncias da Atividade Fı´sica e Esportes – ICAFE, Universidade Cruzeiro do Sul, Rua Galva˜o Bueno, 868, Sa˜o Paulo, SP 01506-000, Brazil. Tel.: +55 11 3385 3103. E-mail addresses: [email protected], [email protected] (P.B. de Freitas). http://dx.doi.org/10.1016/j.ridd.2014.06.002 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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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 gendermatched 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 Sa˜o Paulo, Brazil and recruited from both institutions. Children from the control group were recruited from regular schools in Sa˜o 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).
[(Fig._1)TD$IG]
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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.
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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)TD$IG]
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.
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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 nondyslexic 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
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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 Sa˜o 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. 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