Skip to main content
SpringerLink
Log in

Prefrontal Cortex Activated Bilaterally by a Tilt Board Balance Task: A Functional Near-Infrared Spectroscopy Study in a Semi-Immersive Virtual Reality Environment

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

The aim of this study was to assess the prefrontal cortex (PFC) oxygenation response to a 5-min incremental tilt board balance task (ITBBT) in a semi-immersive virtual reality (VR) environment driven by a depth-sensing camera. It was hypothesized that the PFC would be bilaterally activated in response to the increase of the ITBBT difficulty, given the PFC involvement in the allocation of the attentional resources to maintain postural control. Twenty-two healthy male subjects were asked to use medial–lateral postural sways to maintain their equilibrium on a virtual tilt board (VTB) balancing over a pivot. When the subject was unable to maintain the VTB angle within ±35° the VTB became red (error). An eight-channel fNIRS system was employed for measuring changes in PFC oxygenated-deoxygenated hemoglobin (O2Hb-HHb, respectively). Results revealed that the number of the performed board sways and errors augmented with the increasing of the ITBBT difficulty. A PFC activation was observed with a tendency to plateau for both O2Hb-HHb changes within the last 2 min of the task. A significant main effect of the level of difficulty was found in O2Hb and HHb (p < 0.001). The study has demonstrated that the oxygenation increased over the PFC while the subject was performing an ITBBT in a semi-immersive VR environment. This increase was modulated by the task difficulty, suggesting that the PFC is bilaterally involved in attention-demanding tasks. This task could be considered useful for diagnostic testing and functional neurorehabilitation given its adaptability in elderly and in patients with movement disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anstey KJ, Wood J, Kerr G, Caldwell H, Lord SR (2009) Different cognitive profiles for single compared with recurrent fallers without dementia. Neuropsychology 23:500–508

    Article  PubMed  Google Scholar 

  • Aoki M, Nishihori T, Jiang Y, Nagasaki S, Wakaoka T, Ito Y (2013) Damping control of balance in the medial-lateral direction and the risk of falling in the elderly. Geriatr Gerontol Int 13:182–189

    Article  PubMed  Google Scholar 

  • Atsumori H, Kiguchi M, Katura T, Funane T, Obata A, Sato H, Manaka T, Iwamoto M, Maki A, Koizumi H, Kubota K (2010) Noninvasive imaging of prefrontal activation during attention-demanding tasks performed while walking using a wearable optical topography system. J Biomed Opt 15:046002

    Article  PubMed  Google Scholar 

  • Avola D, Spezialetti M, Placidi G (2013) Design of an efficient framework for fast prototyping of customized human–computer interfaces and virtual environments for rehabilitation. Comput Methods Programs Biomed. http://dx.doi.org/10.1016/j.cmpb.2013.01.009

  • Ayaz H, Shewokis PA, Curtin A, Izzetoglu M, Izzetoglu K, Onaral B (2011) Using MazeSuite and functional near infrared spectroscopy to study learning in spatial navigation. J Vis Exp 56:e3443. doi:10.3791/3443

    Google Scholar 

  • Bandettini P (2007) Functional MRI today. Int J Psychophysiol 63:138–145

    Article  PubMed  Google Scholar 

  • Bauby CE, Kuo AD (2000) Active control of lateral balance in human walking. J Biomech 33:1433–1440

    Article  PubMed  CAS  Google Scholar 

  • Bohil CJ, Alicea B, Biocca FA (2011) Virtual reality in neuroscience research and therapy. Nat Rev Neurosci 12:752–762

    PubMed  CAS  Google Scholar 

  • Borg G (1990) Psychophysical scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health 16:55–58

    Article  PubMed  Google Scholar 

  • Cui X, Bray S, Bryant DM, Glover GH, Reiss AL (2011) A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage 54:2808–2821

    Article  PubMed Central  PubMed  Google Scholar 

  • Cutini S, Scatturin P, Zorzi M (2011) A new method based on ICBM152 head surface for probe placement in multichannel fNIRS. Neuroimage 54:919–927

    Article  PubMed  Google Scholar 

  • Cutini S, Basso Moro S, Bisconti S (2012) Functional near infrared optical imaging in cognitive neuroscience: an introductory review. J Near Infrared Spectrosc 20:75–92

    Article  CAS  Google Scholar 

  • Dieler AC, Tupak SV, Fallgatter AJ (2012) Functional near-infrared spectroscopy for the assessment of speech related tasks. Brain Lang 121:90–109

    Article  PubMed  CAS  Google Scholar 

  • Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251–261

    Article  PubMed  Google Scholar 

  • Duncan A, Meek JH, Clemence M, Elwell CE, Fallon P, Tyszczuk L, Cope M, Delpy DT (1996) Measurement of cranial optical path length as a function of age using phase resolved near infrared spectroscopy. Pediatr Res 39:889–894

    Article  PubMed  CAS  Google Scholar 

  • Eliassen JC, Souza T, Sanes JN (2001) Human brain activation accompanying explicitly directed movement sequence learning. Exp Brain Res 141:269–280

    Article  PubMed  CAS  Google Scholar 

  • Ferrari M, Quaresima V (2012) A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage 63:921–935

    Article  PubMed  Google Scholar 

  • Francis S, Lin X, Aboushoushah S, White TP, Phillips M, Bowtell R, Constantinescu CS (2009) fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage 44(2):469–479

    Article  PubMed  Google Scholar 

  • Gagnon L, Perdue K, Greve DN, Goldenholz D, Kaskhedikar G, Boas DA (2011) Improved recovery of the hemodynamic response in diffuse optical imaging using short optode separations and state-space modeling. Neuroimage 56:1362–1371

    Article  PubMed Central  PubMed  Google Scholar 

  • Gagnon L, Cooper RJ, Yücel MA, Perdue KL, Greve DN, Boas DA (2012) Short separation channel location impacts the performance of short channel regression in NIRS. Neuroimage 59:2518–2528

    Article  PubMed Central  PubMed  Google Scholar 

  • Gagnon L, Yücel MA, Boas DA, Cooper RJ (2013) Further improvement in reducing superficial contamination in NIRS using double short separation measurements. Neuroimage. doi:10.1016/j.neuroimage.2013.01.073

    Google Scholar 

  • Hallacoglu B, Sassaroli A, Fantini S (2013) Optical characterization of two-layered turbid media for non-invasive, absolute oximetry in cerebral and extracerebral tissue. PLoS ONE 8:e64095

    Article  PubMed Central  PubMed  Google Scholar 

  • Holper L, Muehlemann T, Scholkmann F, Eng K, Kiper D, Wolf M (2010) Testing the potential of a virtual reality neurorehabilitation system during performance of observation, imagery and imitation of motor actions recorded by wireless functional near-infrared spectroscopy (fNIRS). J Neuroeng Rehabil 7:57

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoshi Y (2007) Functional near-infrared spectroscopy: current status and future prospects. J Biomed Opt 12:062106

    Article  PubMed  Google Scholar 

  • Huppert T, Schmidt B, Beluk N, Furman J, Sparto P (2012) Measurement of brain activation during an upright stepping reaction task using functional near-infrared spectroscopy. Hum Brain Mapp. doi:10.1002/hbm.22106

    PubMed  Google Scholar 

  • Karim H, Schmidt B, Dart D, Beluk N, Huppert T (2012) Functional near-infrared spectroscopy (fNIRS) of brain function during active balancing using a video game system. Gait Posture 35:367–372

    Article  PubMed Central  PubMed  Google Scholar 

  • Kirilina E, Jelzow A, Heine A, Niessing M, Wabnitz H, Brühl R, Ittermann B, Jacobs AM, Tachtsidis I (2012) The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. Neuroimage 61:70–81

    Article  PubMed Central  PubMed  Google Scholar 

  • Kober SE, Kurzmann J, Neuper C (2012) Cortical correlate of spatial presence in 2D and 3D interactive virtual reality: an EEG study. Int J Psychophysiol 83:365–374

    Article  PubMed  Google Scholar 

  • Kohno S, Miyai I, Seiyama A, Oda I, Ishikawa A, Tsuneishi S, Amita T, Shimizu K (2007) Removal of the skin blood flow artifact in functional near-infrared spectroscopic imaging data through independent component analysis. J Biomed Opt 12:062111

    Article  PubMed  Google Scholar 

  • Kuo AD, Donelan JM (2010) Dynamic principles of gait and their clinical implications. Phys Ther 90:157–174

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee MY, Chang PH, Kwon YH, Jang SH (2013) Differences of the frontal activation patterns by finger and toe movements: a functional MRI study. Neurosci Lett 15(533):7–10

    Article  CAS  Google Scholar 

  • Leff DR, Orihuela-Espina F, Elwell CE, Athanasiou T, Delpy DT, Darzi AW, Yang GZ (2011) Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fNIRS) studies. Neuroimage 54:2922–2936

    Article  PubMed  Google Scholar 

  • Lin PY, Lin SI, Penney T, Chen JJJ (2009) Applications of near infrared spectroscopy and imaging for motor rehabilitation in stroke patients. J Med Biol Eng 29:210–221

    Google Scholar 

  • Loubinoux I, Carel C, Alary F, Boulanouar K, Viallard G, Manelfe C, Rascol O, Celsis P, Chollet F (2001) Within-session and between-session reproducibility of cerebral sensorimotor activation: a test–retest effect evidenced with functional magnetic resonance imaging. J Cereb Blood Flow Metab 21:592–607

    Article  PubMed  CAS  Google Scholar 

  • Meldrum D, Glennon A, Herdman S, Murray D, McConn-Walsh R (2012) Virtual reality rehabilitation of balance: assessment of the usability of the Nintendo Wii® Fit Plus. Disabil Rehabil Assist Technol 7:205–210

    Article  PubMed  Google Scholar 

  • Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S (2007) Sustained prefrontal activation during ataxic gait: a compensatory mechanism for ataxic stroke? Neuroimage 37:1338–1345

    Article  PubMed  Google Scholar 

  • Mihara M, Miyai I, Hatakenaka M, Kubota K, Sakoda S (2008) Role of the prefrontal cortex in human balance control. Neuroimage 43:329–336

    Article  PubMed  Google Scholar 

  • Mihara M, Miyai I, Hattori N, Hatakenaka M, Yagura H, Kawano T, Kubota K (2012) Cortical control of postural balance in patients with hemiplegic stroke. NeuroReport 23:314–319

    Article  PubMed  Google Scholar 

  • Mille ML, Johnson ME, Martinez KM, Rogers MW (2005) Age-dependent differences in lateral balance recovery through protective stepping. Clin Biomech (Bristol, Avon) 20:607–616

    Article  Google Scholar 

  • Miller EK, Freedman DJ, Wallis JD (2002) The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci 357:1123–1136

    Article  PubMed Central  PubMed  Google Scholar 

  • Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N, Hausdorff JM (2011) Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci 66:234–240

    Article  PubMed  Google Scholar 

  • Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, Tsunazawa Y, Suzuki T, Yanagida T, Kubota K (2001) Cortical mapping of gate in humans: a near-infrared spectroscopic topography study. Neuroimage 14:1186–1192

    Article  PubMed  CAS  Google Scholar 

  • Nishihori T, Aoki M, Jiang Y, Nagasaki S, Furuta Y, Ito Y (2012) Effects of aging on lateral stability in quiet stance. Aging Clin Exp Res 24:162–170

    PubMed  Google Scholar 

  • Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Quaresima V, Bisconti S, Ferrari M (2012) A brief review on the use of functional near infrared spectroscopy (fNIRS) for language imaging studies in human newborns and adults. Brain Lang 121:79–89

    Article  PubMed  Google Scholar 

  • Scholkmann F, Kleiser S, Metz A, Zimmermann R, Pavia JM, Wolf U, Wolf M (2013) A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage. doi:10.1016/j.neuroimage.2013.05.004

    PubMed  Google Scholar 

  • Seraglia B, Gamberini L, Priftis K, Scatturin P, Martinelli M, Cutini S (2011) An exploratory fNIRS study with immersive virtual reality: a new method for technical implementation. Front Hum Neurosci 5:176

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Slobounov S, Hallett M, Stanhope S, Shibasaki H (2005) Role of cerebral cortex in human postural control: an EEG study. Clin Neurophysiol 116:315–323

    Article  PubMed  CAS  Google Scholar 

  • Slobounov S, Hallett M, Cao C, Newell K (2008) Modulation of cortical activity as a result of voluntary postural sway direction: an EEG study. Neurosci Lett 442:309–313

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smania N, Corato E, Tinazzi M, Stanzani C, Fiaschi A, Girardi P, Gandolfi M (2010) Effect of balance training on postural instability in patients with idiopathic Parkinson’s disease. Neurorehabil Neural Repair 24:826–834

    Article  PubMed  Google Scholar 

  • Sober SJ, Sabes PN (2003) Multisensory integration during motor planning. J Neurosci 23:6982–6992

    PubMed  CAS  Google Scholar 

  • Srivastava A, Taly AB, Gupta A, Kumar S, Murali T (2009) Post-stroke balance training: role of force platform with visual feedback technique. J Neurol Sci 287:89–93

    Article  PubMed  Google Scholar 

  • Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K (2004) Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23:1020–1026

    Article  PubMed  Google Scholar 

  • Tachibana A, Noah JA, Bronner S, Ono Y, Onozuka M (2011) Parietal and temporal activity during a multimodal dance video game: an fNIRS study. Neurosci Lett 503:125–130

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Takikawa Y, Kawagoe R, Shibuya S, Iwano T, Kitazawa S (2011) Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. Neuroimage 57:991–1002

    Article  PubMed  Google Scholar 

  • Torricelli A, Contini D, Pifferi A, Caffini M, Re R, Zucchelli L, Spinelli L (2013) Time domain functional NIRS imaging for human brain mapping. Neuroimage. doi:10.1016/j.neuroimage.2013.05.106

    PubMed  Google Scholar 

  • van der Meulen M, Allali G, Rieger SW, Assal F, Vuilleumier P (2013) The influence of individual motor imagery ability on cerebral recruitment during gait imagery. Hum Brain Mapp. doi:10.1002/hbm.22192

    Google Scholar 

  • Winter DA (1995) Human balance and posture control during standing and walking. Gait Posture 3:193–214

    Article  Google Scholar 

  • Woollacott M, Shumway-Cook A (2002) Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16:1–14

    Article  PubMed  Google Scholar 

  • Yen CY, Lin KH, Hu MH, Wu RM, Lu TW, Lin CH (2011) Effects of virtual reality-augmented balance training on sensory organization and attentional demand for postural control in people with Parkinson disease: a randomized controlled trial. Phys Ther 91:862–874

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Life, Health and Environmental Sciences, University of L’Aquila, Via Vetoio, 67100, L’Aquila, Italy

    Marco Ferrari, Silvia Bisconti, Matteo Spezialetti, Sara Basso Moro, Caterina Di Palo, Giuseppe Placidi & Valentina Quaresima

Authors
  1. Marco Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silvia Bisconti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matteo Spezialetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sara Basso Moro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Caterina Di Palo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giuseppe Placidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valentina Quaresima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Ferrari.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrari, M., Bisconti, S., Spezialetti, M. et al. Prefrontal Cortex Activated Bilaterally by a Tilt Board Balance Task: A Functional Near-Infrared Spectroscopy Study in a Semi-Immersive Virtual Reality Environment. Brain Topogr 27, 353–365 (2014). https://doi.org/10.1007/s10548-013-0320-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-013-0320-z

Keywords

Search

Navigation