Neuroplastic Effects in Patients With Traumatic Brain Injury After Music-Supported Therapy

Berit Marie Dykesteen Vik, Geir Olve Skeie, Karsten Specht, Berit Marie Dykesteen Vik, Geir Olve Skeie, Karsten Specht

Abstract

Damage to the orbitofrontal cortex (OFC) often occurs following a traumatic brain injury (TBI) and can lead to complex behavioral changes, including difficulty with attention and concentration. We investigated the effects of musical training on patients with behavioral and cognitive deficits following a mild traumatic brain injury (mTBI) and found significant functional neuro-plastic changes in the OFC's networks. The results from neuropsychological tests revealed an improved cognitive performance. Moreover, six out of seven participants in this group returned to work post intervention and reported improved well-being and social behavior. In this study, we explore the functional changes in OFC following music-supported intervention in reference to connecting networks that may be responsible for enhanced social interaction. Furthermore, we discuss the factor of dopamine release during playing as an element providing a possible impact on the results. The intervention consisted of playing piano, two sessions per week in 8 weeks, 30 min each time, with an instructor. Additional playing was required with a minimum of 15 min per day at home. Mean time playing piano in reference to participant's report was 3 h per week during the intervention period. Three groups participated, one mTBI group (n = 7), two control groups consisting of healthy participants, one with music training (n = 11), and one baseline group without music training (n = 12). Participants in the clinical group had received standardized cognitive rehabilitation treatment during hospitalization without recovering from their impairments. The intervention took place 2 years post injury. All participants were assessed with neuropsychological tests and with both task and resting-state functional magnetic resonance imaging (fMRI) pre-post intervention. The results demonstrated a significant improvement of neuropsychological tests in the clinical group, consistent with fMRI results in which there were functional changes in the orbitofrontal networks (OFC). These changes were concordantly seen both in a simple task fMRI but also in resting-state fMRI, which was analyzed with dynamic causal modeling (DCM). We hypothesized that playing piano, as designed in the training protocol, may provide a positive increase in both well-being and social interaction. We suggest that the novelty of the intervention may have clinical relevance for patients with behavioral problems following a TBI.

Keywords: dynamic causal modeling; emotional control; mTBI; music-supported therapy; neuroplasticity; orbitofrontal cortex; social interaction.

Figures

Figure 1
Figure 1
Functional magnetic resonance imaging (fMRI) task. Figure displays the results from the non-parametric analysis on the pre-post differences. The results highlighted areas where patients (P) demonstrated an increase of activity from pre- to post-examination, while control subjects (C; irrespective of music intervention) did not show an increase or even a slight decrease. The results are explored with a non-parametric p-value of p < 0.001. Bar plots show contrast estimates (with 90% confidence interval). OFC, orbitofrontal cortex; MFG, middle frontal gyrus; aIns, anterior insula; ACC, anterior cingulate cortex; SMA, supplementary motor area.
Figure 2
Figure 2
Resting-state dynamic causal modeling (DCM) analysis. Figure displays the overall connectivity of the discovered network in the shaded colors, independent of groups and repetitions. The line thickness for the shaded lines is an indicator of the averaged estimated parameter. Pre-post group differences are displayed in strong colors. Connections, where there was a difference between the patients (P) and the control group with intervention (G1) are displayed with continuous lines, and comparisons to the control group without intervention (G2) are displayed with broken lines. Line thickness inversely scales with the p-values (Note: line thicknesses of the lines in shaded and strong colors are not related and should only illustrate the relative strength of the respective effects).

References

    1. Agnestig C.-B. (1958). Vi Spiller Piano. Stockholm, Sweden: AB Carl Gehrmans Musikforlag.
    1. Balanger H. G., Vanderploeg R. D., Curtiss G., Warden D. L. (2007). Recent neuroimaging techniques in mild traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 19, 5–20. 10.1176/jnp.2007.19.1.5
    1. Brodal H. P., Osnes B., Specht K. (2017). Listening to rhythmic music reduces connectivity within the basal ganglia and the reward system. Front. Neurosci. 11:153. 10.3389/fnins.2017.00153
    1. Brown S., Martinez M., Parsons L. (2006). Music and language side by side in the brain: a PET study of the generation of melodies and sentences. Eur. J. Neurosci. 23, 2791–2803. 10.1111/j.1460-9568.2006.04785.x
    1. Bush G., Luu P., Posner M. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222. 10.1016/s1364-6613(00)01483-2
    1. Chan A. S., Ho Y. C., Cheung M. C. (1998). Music training improves verbal memory. Nature 396:128. 10.1038/24075
    1. Christopher L., Marras C., Duff-Canning S., Koshimori Y., Chen R., Boileau I., et al. . (2013). Combined insular and striatal dopamine dysfunction are associated with executive deficits in Parkinson’s disease with mild cognitive impairment. Brain 137, 565–575. 10.1093/brain/awt337
    1. Clark D. L., Boutros N. N., Mendez M. F. (2018). The Brain and Behavior. Cambridge, MA: Cambridge University Press.
    1. Corbetta M., Patel G., Shulman G. L. (2008). The reorienting system of the human brain: from environment to theory of mind. Neuron 58, 306–324. 10.1016/j.neuron.2008.04.017
    1. Deutsch D. (Ed.) (1982). “Grouping mechanisms in music,” in The Psychology of Music (New York, NY: Academic Press; ), 99–134.
    1. Drapeau J., Gosselin N., Peretz I., McKerral M. (2017). Emotional recognition from dynamic facial, vocal and musical expressions following traumatic brain injury. Brain Inj. 31, 221–229. 10.1080/02699052.2016.1208846
    1. Friston K. J., Kahan J., Biswal B., Razi A. (2014). A DCM for resting state fMRI. Neuroimage 94, 396–407. 10.1016/j.neuroimage.2013.12.009
    1. Goldberg E. (2009). The Executive Brain: Frontal Lobes and the Civilized Mind. New York, NY: Oxford University Press.
    1. Hebb D. (1961). “Distinctive features of learning in the higher animal,” in Brain Mechanisms and Learning, ed. Delafresnaye J. F. (London: Oxford University Press; ), 37–46.
    1. Hegde S. (2014). Music-based cognitive remediation therapy for patients with traumatic brain injury. Front. Neurol. 5:34. 10.3389/fneur.2014.00034
    1. Herholz S. C., Coffey E. B., Pantev C., Zatorre R. J. (2016). Dissociation of neural networks for predisposition and for training-related plasticity in auditory-motor learning. Cereb. Cortex 26, 3125–3134. 10.1093/cercor/bhv138
    1. Heskestad B. (2017). Minimal, Mild and Moderate Traumatic Brain Injury in Rogaland; Guideline Compliance and Early Intervention. Oslo, Norway: University of Oslo; Dr. Philos Doctoral Thesis.
    1. Hugdahl K., Raichle M. E., Mitra A., Specht K. (2015). On the existence of a generalized non-specific task-dependent network. Front. Hum. Neurosci. 9:430. 10.3389/fnhum.2015.00430
    1. Jäncke L. (2009). Music drives brain plasticity. F1000 Biol. Rep. 1:78. 10.3410/b1-78
    1. Kandilarova S., Stayanov D., Kostianev S., Specht K. (2018). Altered resting state effective connectivity of anterior insula in depression. Front. Psychiatry 9:83. 10.3389/fpsyt.2018.00083
    1. Koelsch S., Siebel W. A. (2005). Towards a neural basis of music perception. Trends Cogn. Sci. 9, 578–584. 10.1016/j.tics.2005.10.001
    1. Lehrer J. (2011). The neuroscience of music. Available online at:
    1. Mah L. W. Y., Arnold M. C., Grafman J. (2005). Deficits in social knowledge following damage to ventromedial prefrontal cortex. J. Neuropsychiatry Clin. Neurosci. 17, 66–74. 10.1176/jnp.17.1.66
    1. Menon V., Uddin L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214, 655–667. 10.1007/s00429-010-0262-0
    1. Münthe T. F., Altenmüller E., Jäncke L. (2002). The musician’s brain as a model of neuroplasticity. Nat. Rev. Neurosci. Psychiatry 3, 473–478. 10.1038/nrn843
    1. Nichols T. E., Holmes A. P. (2001). Nonparametric analysis of PET functional neuroimaging experiments: a primer. Hum. Brain Mapp. 15, 1–25. 10.1002/hbm.1058
    1. Nygren-de Boussard C., Holm L. W., Cancelliere C., Godbolt A. K., Boyle E., Stålnacke B. M., et al. . (2014). Nonsurgical interventions after mild traumatic brain injury: a systematic review. Resulsts of the International Collaboration on Mild Traumatic Brain Injury Prognosis. Arch. Phys. Med. Rehabil. 95, S257–S264. 10.1016/j.apmr.2013.10.009
    1. Ockelford A. (1999). The Cognition of Order in Music. A Metacognitive Study. London: The Centre for Advanced Studies in Music Education (ASME) Roehampton Institute London.
    1. Owessen-White C., Belle A. M., Herr N. R., Peele J. L., Gowrishankar P., Carelli R. M., et al. . (2016). Cue-evoked dopamine release rapidly modulates D2 neurons in the nucleus accumbens during motivated behavior. J. Neurosci. 36, 6011–6021. 10.1523/JNEUROSCI.0393-16.2016
    1. Pantev C. (2009). “Auditory-somatosensory integration and cortical plasticity in musical training,” in The Neurosciences and Music III. Disorders and Plasticity. (Boston, MA: The New York Academy of Sciences; ), 131–132.
    1. Parsons L., Sergent J., Hodges D. A., Fox P. T. (2005). The brain basis of Piano performance. Neuropsychologia 43, 199–215. 10.1016/j.neuropsychologia.2004.11.007
    1. Patel A., Peretz I., Tramo M., Labreque R. (1998). Processing prosodic and musical patterns: a neuropsychological investigation. Brain Lang. 61, 123–144. 10.1006/brln.1997.1862
    1. Razi A., Kahan J., Rees G., Friston K. J. (2015). Construct validation of a DCM for resting state fMRI. Neuroimage 106, 1–14. 10.1016/j.neuroimage.2014.11.027
    1. Rolls E. T. (2014). Emotion and Decision-Making Explained. New York, NY: Oxford University Press.
    1. Rudebeck P. H., Mitz A. R., Chacko R. V., Murray E. A. (2013). Effects of amygdala lesions on reward-value coding in orbital and medial prefrontal cortex. Neuron 80, 1519–1531. 10.1016/j.neuron.2013.09.036
    1. Särkamö T., Ripollés P., Vepsäläinen H., Autti T., Silvennoinen H. M., Salli E., et al. . (2014). Structural changes induced by daily music listening in the recovering brain after middle cerebral artery stroke; a voxel-based morphometry study. Front. Hum. Neurosci. 8:245. 10.3389/fnhum.2014.00245
    1. Schlaug G. (2009a). “Listening to and making music facilitates brain recovery processes,” in The Neuroscience and Music III. Disorders and Plasticity, eds Dalla Bella S., Kraus J., Overy K., Pantev C., Snyder J. S., Tervaniemi M., Tillman B., Sclaug G. (Boston, MA: Blackwell on behalf of the New York Academy of Sciences; ), 372–373.
    1. Schlaug G. (2009b). “Music, musicians and brain plasticity,” in The Oxford Handbook of Music Psychology, eds Hallam S., Cross I., Thaut M. H. (New York, NY: Oxford University Press; ), 197–207.
    1. Sigurdardottir S. (2010). A Prospective Study of Traumatic Brain Injury. Oslo: University of Oslo.
    1. Sihvonen A. J., Särkämö T., Leo V., Tervaniemi M., Altenmüller E., Soinila S. (2017). Music-based interventions in neurological rehabilitation. Lancet Neurol. 16, 648–660. 10.1016/S1474-4422(17)30168-0
    1. Stewart L. (2008). Do musicians have different brains? Clin. Med. 8, 304–308. 10.7861/clinmedicine.8-3-304
    1. Thaut M. H. (2010). Neurologic music therapy in cognitive rehabilitation. Music Percept. 27, 281–285. 10.1525/mp.2010.27.4.281
    1. Tramo M. J. (2001). Music of the hemispheres. Science 291, 54–56. 10.1126/science.10.1126/SCIENCE.1056899
    1. Vik B. M. D., Skeie G. O., Vikane E., Specht K. (2018). Effects of music production on cortical plasticity within cognitive rehabilitation of patients with mild traumatic brain injury. Brain Inj. 32, 634–643. 10.1080/02699052.2018.1431842
    1. Vikane E. (2016). Effect of Multidisciplinary Outpatient Treatment After Mild Traumatic Brain Injury. A Randomised Controlled Trial and Prognostic Factor for Return to Work (PhD). Norway: University of Bergen.
    1. Winkler A. M., Ridgway G. R., Webster M. A., Smith S. M., Nichols T. E. (2014). Permutation inference for the general linear model. Neuroimage 92, 381–397. 10.1016/j.neuroimage.2014.01.060
    1. Zald D., Raucht S. (2010). The orbitofrontal cortex Available online at: 10.1093/acprof:oso/9780198565741.001.0001
    1. Zatorre R. (2007). “Neural specialiation for tonal processing,” in The Cognitive Neuroscience of Music, eds Perez I., Zatorre R. (Oxford: Oxford University Brain; ), 231–244.

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