Accepted Manuscript Deviation of the fully protracted tongue: Is it a reliable indicator for language cerebral dominance? Jamaledin Abu Ghaida, Saleh Bani Hani, Ayman Mustafa, Qasim Eldwairi PII: DOI: Reference:
S0306-9877(14)00218-7 http://dx.doi.org/10.1016/j.mehy.2014.05.014 YMEHY 7613
To appear in:
Medical Hypotheses
Received Date: Accepted Date:
4 February 2014 23 May 2014
Please cite this article as: J.A. Ghaida, S.B. Hani, A. Mustafa, Q. Eldwairi, Deviation of the fully protracted tongue: Is it a reliable indicator for language cerebral dominance?, Medical Hypotheses (2014), doi: http://dx.doi.org/ 10.1016/j.mehy.2014.05.014
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Deviation of the fully protracted tongue: Is it a reliable indicator for language cerebral dominance?
Jamaledin Abu Ghaida¹, MD, PhD, Saleh Bani Hani¹, MD, PhD, Ayman Mustafa¹, DDS, PhD and Qasim Eldwairi1, MD, PhD ¹Department of Anatomy, Faculty of Medicine, University of Science and Technology, P.O.Box 3030, 22110 Irbid, Jordan
Corresponding author: Dr. Jamaledin Abu Ghaida Department of Anatomy Faculty of Medicine University of Science and Technology P.O.Box 3030 22110 Irbid, Jordan E-mail:
[email protected]
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Abstract Since its introduction in 1960, The Wada test has been considered the gold standard for language lateralization prior to ablative brain surgery. Due to the invasive nature of The Wada test several noninvasive techniques have been alternatively adopted. Recently, it has been suggested that the tongue deviates toward the language dominant cerebral hemisphere on full protraction. This suggestion is based on the important role the tongue plays in articulation and on the close anatomical relationship between the cortical tongue motor area and the motor speech area. It was proposed that this phenomenon could serve as a reliable and simple method for language brain lateralization. However, this hypothesis is still open for verification. In an attempt to correlate tongue deviation and language cerebral dominance we present and discuss in this paper the results of a study conducted on 339 free adult Jordanian volunteers. Tongue deviation and handedness were determined and statistically correlated. Our results showed that 62% of test subjects did not show any tongue deviation on full protrusion. Additionally, 9% of test subjects showed left-sided tongue deviation on full protraction in spite of 90% right handedness with presumed left language dominant cerebral hemisphere. We conclude that, at least in Jordanians, tongue deviation cannot be considered as a reliable indicator for language lateralization.
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Introduction The importance of language lateralization prior to neurosurgical procedures i.e. resection delineation is self-evident. The Wada test was introduced in 1960 (1). This invasive technique depends on intracarotidamobarbital selective cortical anesthesia. It has long been considered the gold standard for determining language lateralization. Direct cortical stimulation, another invasive technique, offers more localization potential (2). However, the use of the Wada test has been questioned and criticized (3). Consequently, non-invasive procedures such as magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) have been advocatedby many centers. The outcome of these non invasive techniques showed encouraging concordance rates with the Wada test (4). Nevertheless, serious limitations of these procedures have been described and published (5, 6). In an interesting paper published recently, Han and Lee (7) proposed the use of the asymmetry ofthe fully protracted tongueas a simple non-invasive test for language cerebral dominance, which could be adopted as a substitution of the Wada test. The authors argued that the spatial relation of the primary cortical motor area of the genioglossus muscle of the tongue to the Broca’s area and the important role the tongue plays in language add to the validity of the test. Moreover, the authors also suggested that this phenomenon is present in every person and cannot be shifted by cultural or social pressures. However, the authors recognized the need for practical verification of their hypothesis. Our study puts the suggested hypothesis into examination. Materials and Methods A total number of randomly-selected 339 Jordanian adults were recruited for this study. The test subjects were free volunteers of the students of the Jordan University of Science and Technology (JUST), aged 18-23 years, Male: Female ratio was 63.3%:36.7% Deviation of the fully protracted tongue and handedness were determined by three independent trained staff members at the Faculty of Medicine at JUST. The examiners were all medical doctors familiar with thorough clinical physical examination. Tongue deviation was determined by visual comparison between the midline of the face and the direction of the median longitudinal sulcus of the tongue. The examiners always reached consensus regarding the presence or absence of deviation and 3
the direction of deviation if present. The test subjects were additionally questioned about past shifting of handedness. Results were subjected to Chi square statistical analysis for determination of significant correlation (P<0.05). This was performed using SPSS (statistical package for social sciences)software. Results (Table 1) Handedness The number of right-handed subjects was 301(90.1%) whereas the number of left-handed subjects was 27 (8.2%). On the hand, the number of bidexter subjects was 4 (1.7%). Subjects who reported shifting of handedness (left to right) were 7 (2%). This number was excluded from the total number of subjects included in our study ending up with 332 total number of test individuals. Tongue deviation 205 subjects (61.7%) showed no tongue deviation on full protraction whereas 97 subjects (29.2%) showed right-sided tongue deviation. This number constitutes 76% of total individuals with tongue deviation. On the hand, 30 individuals (9.0%) showed left-sided tongue deviation on full protraction.This number constitutes 24% of total individuals with tongue deviation. Correlation test Chi Square Test showed no significant correlation between tongue deviation and handedness (P-value = o.437)
Discussion Along the quest for a simple and non-invasive technique for the determination of language lateralization mild tongue deviation on full protraction has been proposed to be a valid option (7). In the latter paper, the authors suggested that the fully protracted tongue deviates towards the language-dominant cerebral hemisphere. They discussed different interesting aspects and presented valuable data in favor of their hypothesis. They stated that deviation of the fully protracted tongue is present in every person and cannot be shifted by cultural or social pressures as compared to handedness. In this regard, Han and Lee argued that the contralateral corticobulbar fibers related to the genioglossus muscle originate from the inferior part of the precentralgyrus which is closely related to the Broca's area. Consequently, the action of the genioglossus muscle i.e. protrusion of the tongue could be assumed to exhibit a trait of asymmetry similar to the Broca's area. Taking this into consideration, slight midline deviation of fully protracted tongue can be expected to point out to the dominant genioglossus muscle which can indicate the language- dominant hemisphere. 4
Although diverse neuroanatomical and neurophysiological studies could indeed support this hypothesis, nevertheless, several aspects in the literature together with our findings could be interpreted otherwise. It is well documented that the motor cortical area responsible for the movement of the tongue in the lower part of the contralateral motor cortex lies in close anatomical and synaptofunctional proximity to the Broca’s area in humans and other species (8 - 12). Moreover, the hypoglossal nucleus was shown to receive bilateral cortical input except for the part of the nucleus innervating genioglossus muscle, which probably receives contralateral innervation (13). This pathway could suggest that the dominant cerebral hemisphere overrides the non-dominant hemisphere eliciting stronger input to the contralateral hypoglossal nucleus. As a result, the tongue deviates towards the side of the dominant hemisphere. This view could represent the backbone of the hypothesis of Han and Lee. However, the pattern of corticonuclear innervation for motor nuclei is mostly indirect via reticular formation (8, 14). Interestingly, tongue contraction in humans has been shown to be associated with increased activity in the thalamus, cerebellum, basal ganglia, hypothalamus, and midbrain nuclei (10,11). Moreover, in the rat, somatic and visceral centers control the activity of hypoglossal nucleus (15 -18). This makes it impossible to rule out a possible regulating and modifying role of these centers resulting in more balanced tongue contraction. In favor of this possible modifying role speaks the finding that extensive intracortical and subcortical connections of the tongue corticobulbar fibers exist in both humans and other primates (13). Indeed 62% of our test subjects showed no tongue deviation. However, it remains probable that some tongue deviation to either side can be detected using more precise examination techniques e.g. photo and an imposed saggital plane. It is unlikely that such minor degree of deviation may possess any clinical significance. The left cerebral hemisphere is the language dominant hemisphere in about 95% of right handed people. Whereas in left handed people, the left cerebral hemisphere is the language dominant hemisphere in about 75% (19). However, only 9% of our test subjects showed tongue deviation to the left. This obvious discrepancy significantly argues against the hypothesisof Han and Lee. Our findings are supported by a previous study where tongue deviation was documented in only 5% of test subjects (20). The interesting complex nature of this subject is further highlighted by correlating tongue deviation to handedness. Handedness is the most obvious behavioral asymmetry in man with 90% right handed. The remaining 10% are left handed, or bidexters with no preference (21). Handedness is closely associated with hemisphere language dominance and can be used, as we did in our study, as a rough indicator of cerebral hemisphere dominance (22). We do acknowledge the limited validity of referring to handedness as a correlate of cerebral hemisphere dominance in clinical practice. Surgeons do not rely on the patients reported handedness as a language lateralization determinant. Surgeons preferably rely on fMRI as a less invasive alternative to the Wada test (4).In the same context, tongue deviation cannot be adopted unless a direct comparison between the Wada test and these parameters has been made. Nevertheless, the whole profile of our data cannot be ignored. In accordance with published data (21), 90% of our test subjects were right-handed, but only 24% of those who exhibited tongue deviation showed left-sided deviation. Assuming a general trend of contralateral cerebral hemisphere dominance 5
in relation to handedness, approximately 90% of our test subjects have left-sided dominant cerebral hemisphere. If tongue deviation on protrusion would point to the dominant hemisphere, as Han and Lee (7) hypothesized, one would expect to confirm left-sided tongue deviation in the vast majority of individuals. On the contrary, almost two thirds of our test subjects showed no deviation. The majority of the individualswho exhibited deviation of protruded tongue showed right-sided deviation i.e. towards the non-dominant hemisphere. Statistical analysis of our data confirmed the absence of a significant correlation between patterns of handedness and tongue deviation. In conclusion, our results strongly argue against the proposed hypothesis of Han and Lee (7). At least in Jordanians, tongue deviation can neither be considered as an indication of the dominant cerebral hemisphere, nor as an indicator of language lateralization. Conflicts of Interest: None declared.
References 1. The Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance: experimental and clinical observations. J Neurosurg 17: 266-282 2. Penfield W, Jasper HH (1954) Epilepsy and the Functional Anatomy of the Human Brain, 1st Edition. Boston: Little, xv-896 3. Baxendale S, Thompson PJ, Duncan JS (2008), The role of the The Wada test in the surgical treatment of temporal lobe epilepsy: An international survey. Epilepsia 49: 715-720 4. Swanson SJ, Sabsevitz DS, Hammeke TA, Binder RJ (2007) Functional magnetic resonance imaging of language in epilepsy. Neuropsychol Rev 17: 491-504 5. Arora J, Pugh K, Westerveld M, Spencer S, Spencer DD, Todd Constable R (2009), Language lateralization in epilepsy patients: fMRI validated with the The Wada procedure. Epilepsia 50(10): 22252241 6. Wellmer J, Weber B, Urbach H, Reul J, Fernandez G, Elger CE (2009), Cerebral lesions can impair fMRI based language lateralization. Epilepsia 50(10): 2213-2224 7. Han D-G, Lee Y-H (2010) Asymmetry of protracted tongue: Can it replace the The Wada test? Medical Hypotheses 74: 782-783 8. Alipour M, Chen Y, Juergens U (1997) Anterograde projections of the cortical tongue area in the tree shrew (Tupaiabelangeri). J Hirnforsch 38(3): 405-423
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9. Meyer B-U, Liebsch R, Roericht S (1997) Tongue motor responses following transcranial magnetic stimulation of the motor cortex and proximal hypoglossal nerve in man. Electroencephalography and Clinical Neurophysiology/Electromyography and Motor Control 105(1): 15-23 10. Corfield DR, Murphy K, Josephs O, Fink GR, Frackowiak RSJ, Guz A, Adams L, Turner R (1999) Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. J ApplPhysiol 86: 1468-1477 11. Alipour M, Chen Y, Juergens U (2002) Anterograde projections of the motorcortical tongue area in the saddle-back tamarin (Saguinusfuscicollis). Brain BehavEvol 60(2) 101-116 12. Juergens U, Alipour M (2002) A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neurosci let. 328(3): 245-248 13. Urban pp, Hopf HC, Connemann B, Hundemer HP, Koehler J (1996) The course of cortico-hypoglossal projections in the human brainstem. Brain 119(3): 1031-1038 14. Borke RC, Nau ME, Ringler RL Jr. (1983) Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269(1): 47-55 15. Yang CCH, Chan JYH, Chan SHH (1995) Excitatory innervation of caudal hypoglossal nucleus from nucleus reticularisgigantocellularis in the rat. Neuroscience 65(2): 365-374 16. Sawczuk A, Mosier KM (2001) Neural control of tongue movement with respect to respiration and swallowing. Critical Reviews in Oral Biology and Medicine 12(1): 18-37 17. Wilson-Pauwels L, Akesson EJ, Stewart PA, Spacey SD (2002) Cranial nerves in health and disease. 2nd ed. BC Decker Inc. p. 216-225 18. Lin HC, Barkhaus PE (2009) Cranial nerve XII: the hypoglossal nerve. SeminNeurol 29(1): 45-52 19. Van der Haegen L, Cai Q, Brysbaert M (2012). Colateralization of Broca's area and the visual word form area in left-handers: fMRI evidence. Brain Lang. 122(3):171-178 20. Umapathi T, Venketasubramanian N, leck KJ, Tan CB, Lee WL, Tjia H (2000) Tongue deviation in acute ischemic stroke: A study of supranuclear twelfth cranial nerve palsy in 300 stroke patients. Cerebrovasc Dis 10(6): 462-465 21. Rothi LJ, Heilman KM (1997) Apraxia: the neurophysiology of action (brain damage, behavior and cognition). 1st ed. Psychology Press, p. 19-28 22. Lishman WA, McMeekan ERL (1977) Handedness in relation to direction and degree of cerebral dominance for language. Cortex 13: 30-43
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Table 1
Handedness Right Handers Left Handers Bidexters Total
No Deviation 187 (62.1%) 15 (55.6%) 3 (75%) 205 (61.7%)
Tongue Deviation Right Deviation 89 (29.6%) 8 (29.6%) 0 (0%) 97 (29.2%)
Total Left Deviation 25 (8.3%) 4 (14.8%) 1 (25%) 30 (9%)
301 27 4 332
P-value
0.437
Legend to Table 1 Number of volunteers classified according to handedness and tongue deviation. Percentages represent relative number of individuals with one direction of tongue deviation as compared to the total number of test subjects exhibiting one type of handedness within each row. Significant correlation: P-value < 0.05
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Abstract Since its introduction in 1960, The Wada test has been considered the gold standard for language lateralization prior to ablative brain surgery. Due to the invasive nature of The Wada test several noninvasive techniques have been alternatively adopted. Recently, it has been suggested that the tongue deviates toward the language dominant cerebral hemisphere on full protraction. This suggestion is based on the important role the tongue plays in articulation and on the close anatomical relationship between the cortical tongue motor area and the motor speech area. It was proposed that this phenomenon could serve as a reliable and simple method for language brain lateralization. However, this hypothesis is still open for verification. In an attempt to correlate tongue deviation and language cerebral dominance we present and discuss in this paper the results of a study conducted on 339 free adult Jordanian volunteers. Tongue deviation and handedness were determined and statistically correlated. Our results showed that 62% of test subjects did not show any tongue deviation on full protrusion. Additionally, 9% of test subjects showed left-sided tongue deviation on full protraction in spite of 90% right handedness with presumed left language dominant cerebral hemisphere. We conclude that, at least in Jordanians, tongue deviation cannot be considered as a reliable indicator for language lateralization.
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Conflict of Interest The authors declare that they have no conflict of interest
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