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Attentional asymmetry or laterality of motor control? Commentary on Buckingham et al. (this issue)
c o r t e x 4 7 ( 2 0 1 1 ) 5 0 9 e5 1 0
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/cortex
Discussion forum
Attentional asymmetry or laterality of motor control? Commentary on Buckingham et al. (this issue)5 Iraj Derakhshan* Case Western Reserve and Cincinnati Universities School of Medicine, Ohio, USA
It has been nearly four decades since researchers have identified the role of the anterior portion of the corpus callosum in activating the nondominant hemisphere for moving the contralateral (i.e., nondominant) side of the body; utilizing the commands issued for that purpose in the dominant hemisphere (Preilowski, 1972). Recently, the relationship of the laterality of major hemisphere (command center or action hemisphere) to behavioral handedness has been the subject of an intense study (Derakhshan, 2006a, 2009). According to the newly described one-way callosal traffic circuitry, all commands are issued in same hemisphere, regardless of the laterality of the effector(s) intended for implementing those commands. However, approximately one in five persons in society at large claim a handedness opposite for which the person is wired (they speak with the hemisphere ipsilateral to their behavioral handedness). Vast majority of such people with “atypical brainedness” are among those who claim to be left handed (Gonzalez and Goodale, 2009). In contrast, only about 20% of right handers are incongruous in their laterality of command center (or speech hemisphere) and their behavioral handedness (i.e., they speak with their right hemisphere) (Thomson et al., 1998; Derakhshan, 2006a, 2006b). To sum, anyone capable of holding a pen in each hand and draw a line with both hands simultaneously will note a difference between performances of the two hands. It has been documented that the hand opposite to the command center draws lines that are longer and straighter compared to those drawn by the nondominant hand (regardless of the behavioral handedness of the subject) (Derakhshan, 2009). This disparity of performance (i.e., the wider excursion of the neurally dominant side), which is also evident in moving the eyes to the sides and in movements of the diaphragms (Derakhshan, 2005; Kiryu et al., 2006), is the result of the proximity of the dominant side of the body to the command 5
center by a callosum width (i.e., by an interhemispheric transfer time e IHTT). The test may also be performed with the eyes closed, a modification that removes the role of “attention” as a confounding and confusing factor. Clearly, the inferiority of the performance of the nondominant hand is the result of degradation of the command signal as it moves from the command center to the minor hemisphere; resulting in the well documented trajectory distortion and variability of the performance of the nondominant side of the body (Summers, 1995; Freitas and Schotz, 2009). Turning to the article by Buckingham et al. (this issue), this expected discrepancy between neural and behavioral handedness (see above) among the right handed participants in that study appeared in Fig. 4a, wherein 3 of 17 participants had higher right hand cue costs compared to the remaining 14 (who displayed the opposite features). Also to be noted was that right handers as a group showed a delay of 20 msec in their left hands performances when responding to visual stimuli compared to the right hand (page 6), reflecting the inevitable IHTT. The fact that half of left handers are wired as right handers (left hemispheric in laterality of command center) has been documented in the past using the simple reaction time (Derakhshan, 2006a, 2006b). Recently Gonzalez and Goodale (2009) documented that visual control of precision grasping and language is controlled by the same hemisphere. The same discovery was made by Elias et al. using a reaction time paradigm (Elias et al., 1999). In the past, cases showing discrepancy of behavioral and neural handedness, evidenced by an unexpected delay of the right side in an avowed right hander, has been labeled as “idiosyncratic” (Honda, 2002; Coubard and Kapoula, 2008; Derakhshan, 2004), referred to as cases of crossed right hemispheric syndrome (Marchetti et al., 2005) or were simply
Dedication: The author dedicates this note to the memory of his beloved sister, Farkhondeh Derakhshan, Melbourne Australia. * Corresponding author. 415 Morris St, Charleston, WV, USA. E-mail address: [email protected]. 0010-9452/$ e see front matter ª 2010 Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2010.11.012
510
c o r t e x 4 7 ( 2 0 1 1 ) 5 0 9 e5 1 0
ignored [such as in the article presently under discussion (Fig. 4)]. It is of historical interest that Liepmann’s Imperial Counselor, who had no aphasia or hemiplegia, was apraxic on his right belonged to the same “exceptional” group of subjects referred to above (Jeannerod, 2006). Another famous “fake hander,” was the renowned neuroanatomist Brodal (1973). In an influential self-portrait of a stroke involving his right hemisphere, Brodal documented the occurrence of aphasia in his own written speech (using the right hand). In Brodal’s words, this was characterized by “skipping or doubling of letters, etc., related to language functions.” The one-way callosal traffic circuitry (underpinning laterality of motor and sensory control, based on the directionality of callosal traffic in a person) provides a verifiable explanation for the above-mentioned neuro-behavioral inconsistencies. The methodology adopted by Buckingham et al. (2011, this issue) does provide quantitative information concerning the same topic (see above), comparable to the bimanual simultaneous drawing test.
references
Brodal A. Self observations and neuroanatomical considerations after a stroke. Brain, 96(4): 675e694, 1973. Buckingham G, Main GC, and Carey DP. Asymmetries in motor attention during a cued bimanual reaching task: Left and right handers compared. Cortex, 47(4): 432e440, 2011. Coubard OA and Kapoula Z. Saccades during symmetrical vergence. Graefe’s Archive for Clinical and Experimental Ophthalmology, 246(4): 521e536, 2008. Derakhshan I. Handedness and macular vision: Laterality of motor control underpins both. Neurological Research, 26: 331e337, 2004. Derakhshan I. Crossed Uncrossed Difference (CUD) in a new light: Anatomy of the negative CUD in Poffenberger’s paradigm. Acta Neurologica Scandinavica, 113: 203e208, 2006a. Derakhshan I. Right sided weakness with right subdural hematoma: Motor deafferentation of the left hemisphere resulted in paralysis of the right side. Brain Injury, 23: 770e774, 2009.
Derakhshan I. How do the eyes move together? New understandings help explain eye movement in patients with stroke. Canadian Medical Association Journal, 172: 171e173, 2005. Derakhshan I. Laterality of seizure onset and the simple reaction time: Revamping the Poffenberger paradigm for seizure surgery. Neurological Research, 28: 777e784, 2006b. Elias LJ, Bulman-Fleming MB, and McManus IC. Visual temporal asymmetries are related to asymmetries in linguistic perception. Neuropsychologia, 37(11): 1243e1249, 1999. Freitas SM and Schotz JP. Does hand dominance affect the use of motor abundance when reaching to uncertain targets? Human Movement Science, 28(2): 169e190, 2009. Gonzalez CL and Goodale MA. Hand preference for precision grasping predicts language lateralization. Neuropsychologia, 47(14): 3182e3189, 2009. Honda H. Idiosyncratic left-right asymmetries of saccadic latencies: Examination in a gap paradigm. Vision Research, 42: 1437e1445, 2002. Jeannerod M. The origin of voluntary action. History of a physiological concept. Comptes Rendus, Biologies, 329(5e6): 354e362, 2006. Kiryu S, Loring H, Mori Y, Rofski NM, Hatabu H, and Takahashi M. Quantitative analysis of the velocity and synchronicity of diaphragmatic motion: Dynamic MRI in different postures. Magnetic Resonance Imaging, 24(10): 1325e1332, 2006. Marchetti C, Carey D, and Della Sala S. Crossed right hemisphere syndrome following left thalamic stroke. Journal of Neurology, 252(4): 401e411, 2005. Preilowski BF. Possible contribution of the anterior forebrain commissures to bilateral motor coordination. Neuropsychologia, 10(3): 267e277, 1972. Summers JJ. Going around in circles: The dynamics of bimanual circling. In Glencross DJ and Piek PJ (Eds), Motor Control and Sensory Motor Coordination: Issues and Directions. Elsevier Science, 1995: 231e253. Thomson AM, Taylor R, and Whittle IR. Assessment of communication impairment and the effects of resective surgery in solitary, right-sided supratentorial intracranial tumours: A prospective study. British Journal of Neurosurgery, 12(5): 423e429, 1998.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/cortex
Discussion forum
Attentional asymmetry or laterality of motor control? Commentary on Buckingham et al. (this issue)5 Iraj Derakhshan* Case Western Reserve and Cincinnati Universities School of Medicine, Ohio, USA
It has been nearly four decades since researchers have identified the role of the anterior portion of the corpus callosum in activating the nondominant hemisphere for moving the contralateral (i.e., nondominant) side of the body; utilizing the commands issued for that purpose in the dominant hemisphere (Preilowski, 1972). Recently, the relationship of the laterality of major hemisphere (command center or action hemisphere) to behavioral handedness has been the subject of an intense study (Derakhshan, 2006a, 2009). According to the newly described one-way callosal traffic circuitry, all commands are issued in same hemisphere, regardless of the laterality of the effector(s) intended for implementing those commands. However, approximately one in five persons in society at large claim a handedness opposite for which the person is wired (they speak with the hemisphere ipsilateral to their behavioral handedness). Vast majority of such people with “atypical brainedness” are among those who claim to be left handed (Gonzalez and Goodale, 2009). In contrast, only about 20% of right handers are incongruous in their laterality of command center (or speech hemisphere) and their behavioral handedness (i.e., they speak with their right hemisphere) (Thomson et al., 1998; Derakhshan, 2006a, 2006b). To sum, anyone capable of holding a pen in each hand and draw a line with both hands simultaneously will note a difference between performances of the two hands. It has been documented that the hand opposite to the command center draws lines that are longer and straighter compared to those drawn by the nondominant hand (regardless of the behavioral handedness of the subject) (Derakhshan, 2009). This disparity of performance (i.e., the wider excursion of the neurally dominant side), which is also evident in moving the eyes to the sides and in movements of the diaphragms (Derakhshan, 2005; Kiryu et al., 2006), is the result of the proximity of the dominant side of the body to the command 5
center by a callosum width (i.e., by an interhemispheric transfer time e IHTT). The test may also be performed with the eyes closed, a modification that removes the role of “attention” as a confounding and confusing factor. Clearly, the inferiority of the performance of the nondominant hand is the result of degradation of the command signal as it moves from the command center to the minor hemisphere; resulting in the well documented trajectory distortion and variability of the performance of the nondominant side of the body (Summers, 1995; Freitas and Schotz, 2009). Turning to the article by Buckingham et al. (this issue), this expected discrepancy between neural and behavioral handedness (see above) among the right handed participants in that study appeared in Fig. 4a, wherein 3 of 17 participants had higher right hand cue costs compared to the remaining 14 (who displayed the opposite features). Also to be noted was that right handers as a group showed a delay of 20 msec in their left hands performances when responding to visual stimuli compared to the right hand (page 6), reflecting the inevitable IHTT. The fact that half of left handers are wired as right handers (left hemispheric in laterality of command center) has been documented in the past using the simple reaction time (Derakhshan, 2006a, 2006b). Recently Gonzalez and Goodale (2009) documented that visual control of precision grasping and language is controlled by the same hemisphere. The same discovery was made by Elias et al. using a reaction time paradigm (Elias et al., 1999). In the past, cases showing discrepancy of behavioral and neural handedness, evidenced by an unexpected delay of the right side in an avowed right hander, has been labeled as “idiosyncratic” (Honda, 2002; Coubard and Kapoula, 2008; Derakhshan, 2004), referred to as cases of crossed right hemispheric syndrome (Marchetti et al., 2005) or were simply
Dedication: The author dedicates this note to the memory of his beloved sister, Farkhondeh Derakhshan, Melbourne Australia. * Corresponding author. 415 Morris St, Charleston, WV, USA. E-mail address: [email protected]. 0010-9452/$ e see front matter ª 2010 Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2010.11.012
510
c o r t e x 4 7 ( 2 0 1 1 ) 5 0 9 e5 1 0
ignored [such as in the article presently under discussion (Fig. 4)]. It is of historical interest that Liepmann’s Imperial Counselor, who had no aphasia or hemiplegia, was apraxic on his right belonged to the same “exceptional” group of subjects referred to above (Jeannerod, 2006). Another famous “fake hander,” was the renowned neuroanatomist Brodal (1973). In an influential self-portrait of a stroke involving his right hemisphere, Brodal documented the occurrence of aphasia in his own written speech (using the right hand). In Brodal’s words, this was characterized by “skipping or doubling of letters, etc., related to language functions.” The one-way callosal traffic circuitry (underpinning laterality of motor and sensory control, based on the directionality of callosal traffic in a person) provides a verifiable explanation for the above-mentioned neuro-behavioral inconsistencies. The methodology adopted by Buckingham et al. (2011, this issue) does provide quantitative information concerning the same topic (see above), comparable to the bimanual simultaneous drawing test.
references
Brodal A. Self observations and neuroanatomical considerations after a stroke. Brain, 96(4): 675e694, 1973. Buckingham G, Main GC, and Carey DP. Asymmetries in motor attention during a cued bimanual reaching task: Left and right handers compared. Cortex, 47(4): 432e440, 2011. Coubard OA and Kapoula Z. Saccades during symmetrical vergence. Graefe’s Archive for Clinical and Experimental Ophthalmology, 246(4): 521e536, 2008. Derakhshan I. Handedness and macular vision: Laterality of motor control underpins both. Neurological Research, 26: 331e337, 2004. Derakhshan I. Crossed Uncrossed Difference (CUD) in a new light: Anatomy of the negative CUD in Poffenberger’s paradigm. Acta Neurologica Scandinavica, 113: 203e208, 2006a. Derakhshan I. Right sided weakness with right subdural hematoma: Motor deafferentation of the left hemisphere resulted in paralysis of the right side. Brain Injury, 23: 770e774, 2009.
Derakhshan I. How do the eyes move together? New understandings help explain eye movement in patients with stroke. Canadian Medical Association Journal, 172: 171e173, 2005. Derakhshan I. Laterality of seizure onset and the simple reaction time: Revamping the Poffenberger paradigm for seizure surgery. Neurological Research, 28: 777e784, 2006b. Elias LJ, Bulman-Fleming MB, and McManus IC. Visual temporal asymmetries are related to asymmetries in linguistic perception. Neuropsychologia, 37(11): 1243e1249, 1999. Freitas SM and Schotz JP. Does hand dominance affect the use of motor abundance when reaching to uncertain targets? Human Movement Science, 28(2): 169e190, 2009. Gonzalez CL and Goodale MA. Hand preference for precision grasping predicts language lateralization. Neuropsychologia, 47(14): 3182e3189, 2009. Honda H. Idiosyncratic left-right asymmetries of saccadic latencies: Examination in a gap paradigm. Vision Research, 42: 1437e1445, 2002. Jeannerod M. The origin of voluntary action. History of a physiological concept. Comptes Rendus, Biologies, 329(5e6): 354e362, 2006. Kiryu S, Loring H, Mori Y, Rofski NM, Hatabu H, and Takahashi M. Quantitative analysis of the velocity and synchronicity of diaphragmatic motion: Dynamic MRI in different postures. Magnetic Resonance Imaging, 24(10): 1325e1332, 2006. Marchetti C, Carey D, and Della Sala S. Crossed right hemisphere syndrome following left thalamic stroke. Journal of Neurology, 252(4): 401e411, 2005. Preilowski BF. Possible contribution of the anterior forebrain commissures to bilateral motor coordination. Neuropsychologia, 10(3): 267e277, 1972. Summers JJ. Going around in circles: The dynamics of bimanual circling. In Glencross DJ and Piek PJ (Eds), Motor Control and Sensory Motor Coordination: Issues and Directions. Elsevier Science, 1995: 231e253. Thomson AM, Taylor R, and Whittle IR. Assessment of communication impairment and the effects of resective surgery in solitary, right-sided supratentorial intracranial tumours: A prospective study. British Journal of Neurosurgery, 12(5): 423e429, 1998.