Skip to main content
Top
Published in: Brain Structure and Function 2/2018

01-03-2018 | Original Article

Neuroanatomical correlates of haptic object processing: combined evidence from tractography and functional neuroimaging

Authors: Haemy Lee Masson, Hyeok-mook Kang, Laurent Petit, Christian Wallraven

Published in: Brain Structure and Function | Issue 2/2018

Login to get access

Abstract

Touch delivers a wealth of information already from birth, helping infants to acquire knowledge about a variety of important object properties using their hands. Despite the fact that we are touch experts as much as we are visual experts, surprisingly, little is known how our perceptual ability in touch is linked to either functional or structural aspects of the brain. The present study, therefore, investigates and identifies neuroanatomical correlates of haptic perceptual performance using a novel, multi-modal approach. For this, participants’ performance in a difficult shape categorization task was first measured in the haptic domain. Using a multi-modal functional magnetic resonance imaging and diffusion-weighted magnetic resonance imaging analysis pipeline, functionally defined and anatomically constrained white-matter pathways were extracted and their microstructural characteristics correlated with individual variability in haptic categorization performance. Controlling for the effects of age, total intracranial volume and head movements in the regression model, haptic performance was found to correlate significantly with higher axial diffusivity in functionally defined superior longitudinal fasciculus (fSLF) linking frontal and parietal areas. These results were further localized in specific sub-parts of fSLF. Using additional data from a second group of participants, who first learned the categories in the visual domain and then transferred to the haptic domain, haptic performance correlates were obtained in the functionally defined inferior longitudinal fasciculus. Our results implicate SLF linking frontal and parietal areas as an important white-matter track in processing touch-specific information during object processing, whereas ILF relays visually learned information during haptic processing. Taken together, the present results chart for the first time potential neuroanatomical correlates and interactions of touch-related object processing.
Appendix
Available only for authorised users
Footnotes
1
We leave out the VOF in the present paper since our previous study did not show any haptic or visuo-haptic shape processing involvement (Lee Masson et al. 2017).
 
Literature
go back to reference Abe O, Yamasue H, Aoki S, Suga M, Yamada H, Kasai K, Masutani Y, Kato N, Kato N, Ohtomo K (2008) Aging in the CNS: comparison of gray/white matter volume and diffusion tensor data. Neurobiol Aging 29(1):102–116CrossRefPubMed Abe O, Yamasue H, Aoki S, Suga M, Yamada H, Kasai K, Masutani Y, Kato N, Kato N, Ohtomo K (2008) Aging in the CNS: comparison of gray/white matter volume and diffusion tensor data. Neurobiol Aging 29(1):102–116CrossRefPubMed
go back to reference Amedi A, Jacobson G, Hendler T, Malach R, Zohary E (2002) Convergence of visual and tactile shape processing in the human lateral occipital complex. Cereb Cortex 12(11):1202–1212CrossRefPubMed Amedi A, Jacobson G, Hendler T, Malach R, Zohary E (2002) Convergence of visual and tactile shape processing in the human lateral occipital complex. Cereb Cortex 12(11):1202–1212CrossRefPubMed
go back to reference Amedi A, Raz N, Azulay H, Malach R, Zohary E (2010) Cortical activity during tactile exploration of objects in blind and sighted humans. Restor Neurol Neurosci 28(2):143PubMed Amedi A, Raz N, Azulay H, Malach R, Zohary E (2010) Cortical activity during tactile exploration of objects in blind and sighted humans. Restor Neurol Neurosci 28(2):143PubMed
go back to reference Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11(9):3276–3286CrossRefPubMed Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11(9):3276–3286CrossRefPubMed
go back to reference Catani M, Jones DK (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16CrossRefPubMed Catani M, Jones DK (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16CrossRefPubMed
go back to reference Catani M, Allin MP, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK (2007) Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci 104(43):17163–17168CrossRefPubMedPubMedCentral Catani M, Allin MP, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK (2007) Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci 104(43):17163–17168CrossRefPubMedPubMedCentral
go back to reference Coello AF, Duvaux S, De Benedictis A, Matsuda R, Duffau H (2013) Involvement of the right inferior longitudinal fascicle in visual hemiagnosia: a brain stimulation mapping study: case report. J Neurosurg 118(1):202–205CrossRef Coello AF, Duvaux S, De Benedictis A, Matsuda R, Duffau H (2013) Involvement of the right inferior longitudinal fascicle in visual hemiagnosia: a brain stimulation mapping study: case report. J Neurosurg 118(1):202–205CrossRef
go back to reference De Schotten MT, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246CrossRef De Schotten MT, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246CrossRef
go back to reference Deshpande G, Hu X, Stilla R, Sathian K (2008) Effective connectivity during haptic perception: a study using Granger causality analysis of functional magnetic resonance imaging data. Neuroimage 40(4):1807–1814CrossRefPubMedPubMedCentral Deshpande G, Hu X, Stilla R, Sathian K (2008) Effective connectivity during haptic perception: a study using Granger causality analysis of functional magnetic resonance imaging data. Neuroimage 40(4):1807–1814CrossRefPubMedPubMedCentral
go back to reference Farquharson S, Tournier J-D, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A (2013) White matter fiber tractography: why we need to move beyond DTI: clinical article. J Neurosurg 118(6):1367–1377CrossRefPubMed Farquharson S, Tournier J-D, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A (2013) White matter fiber tractography: why we need to move beyond DTI: clinical article. J Neurosurg 118(6):1367–1377CrossRefPubMed
go back to reference Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towards quantitative connectivity analysis: reducing tractography biases. Neuroimage 98:266–278CrossRefPubMed Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towards quantitative connectivity analysis: reducing tractography biases. Neuroimage 98:266–278CrossRefPubMed
go back to reference Greenberg AS, Verstynen T, Chiu Y-C, Yantis S, Schneider W, Behrmann M (2012) Visuotopic cortical connectivity underlying attention revealed with white-matter tractography. J Neurosci 32(8):2773–2782CrossRefPubMedPubMedCentral Greenberg AS, Verstynen T, Chiu Y-C, Yantis S, Schneider W, Behrmann M (2012) Visuotopic cortical connectivity underlying attention revealed with white-matter tractography. J Neurosci 32(8):2773–2782CrossRefPubMedPubMedCentral
go back to reference Gschwind M, Pourtois G, Schwartz S, Van De Ville D, Vuilleumier P (2012) White-matter connectivity between face-responsive regions in the human brain. Cereb Cortex (New York, NY) 22(7):1564–1576 Gschwind M, Pourtois G, Schwartz S, Van De Ville D, Vuilleumier P (2012) White-matter connectivity between face-responsive regions in the human brain. Cereb Cortex (New York, NY) 22(7):1564–1576
go back to reference James TW, Kim S, Fisher JS (2007) The neural basis of haptic object processing. Can J Exp Psychol 61(3):219–229CrossRefPubMed James TW, Kim S, Fisher JS (2007) The neural basis of haptic object processing. Can J Exp Psychol 61(3):219–229CrossRefPubMed
go back to reference Kantarci K, Senjem M, Avula R, Zhang B, Samikoglu A, Weigand S, Przybelski S, Edmonson H, Vemuri P, Knopman D (2011) Diffusion tensor imaging and cognitive function in older adults with no dementia. Neurology 77(1):26–34CrossRefPubMedPubMedCentral Kantarci K, Senjem M, Avula R, Zhang B, Samikoglu A, Weigand S, Przybelski S, Edmonson H, Vemuri P, Knopman D (2011) Diffusion tensor imaging and cognitive function in older adults with no dementia. Neurology 77(1):26–34CrossRefPubMedPubMedCentral
go back to reference Kassuba T, Klinge C, Hölig C, Röder B, Siebner HR (2013) Vision holds a greater share in visuo-haptic object recognition than touch. Neuroimage 65:59–68CrossRefPubMed Kassuba T, Klinge C, Hölig C, Röder B, Siebner HR (2013) Vision holds a greater share in visuo-haptic object recognition than touch. Neuroimage 65:59–68CrossRefPubMed
go back to reference Klatzky RL, Lederman SJ, Metzger VA (1985) Identifying objects by touch: an “expert system”. Percept Psychophys 37(4):299–302CrossRefPubMed Klatzky RL, Lederman SJ, Metzger VA (1985) Identifying objects by touch: an “expert system”. Percept Psychophys 37(4):299–302CrossRefPubMed
go back to reference Lederman SJ, Klatzky RL (2009) Haptic perception: a tutorial. Atten Percept Psychophys 71(7):1439–1459CrossRefPubMed Lederman SJ, Klatzky RL (2009) Haptic perception: a tutorial. Atten Percept Psychophys 71(7):1439–1459CrossRefPubMed
go back to reference Lee Masson H, Bulthé J, Op de Beeck H, Wallraven C (2016) Visual and haptic shape processing in the human brain: unisensory processing, multisensory convergence, and top-down influences. Cereb Cortex 26(8):3402–3412CrossRefPubMed Lee Masson H, Bulthé J, Op de Beeck H, Wallraven C (2016) Visual and haptic shape processing in the human brain: unisensory processing, multisensory convergence, and top-down influences. Cereb Cortex 26(8):3402–3412CrossRefPubMed
go back to reference Lee Masson H, Wallraven C, Petit L (2017) “Can touch this”: Cross‐modal shape categorization performance is associated with microstructural characteristics of white matter association pathways. Hum Brain Mapp 38(2):842–854CrossRefPubMed Lee Masson H, Wallraven C, Petit L (2017) “Can touch this”: Cross‐modal shape categorization performance is associated with microstructural characteristics of white matter association pathways. Hum Brain Mapp 38(2):842–854CrossRefPubMed
go back to reference Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349CrossRefPubMed Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349CrossRefPubMed
go back to reference Peltier S, Stilla R, Mariola E, LaConte S, Hu X, Sathian K (2007) Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception. Neuropsychologia 45(3):476–483CrossRefPubMed Peltier S, Stilla R, Mariola E, LaConte S, Hu X, Sathian K (2007) Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception. Neuropsychologia 45(3):476–483CrossRefPubMed
go back to reference Reed CL, Caselli RJ (1994) The nature of tactile agnosia: a case study. Neuropsychologia 32(5):527–539CrossRefPubMed Reed CL, Caselli RJ (1994) The nature of tactile agnosia: a case study. Neuropsychologia 32(5):527–539CrossRefPubMed
go back to reference Shinoura N, Suzuki Y, Tsukada M, Katsuki S, Yamada R, Tabei Y, Saito K, Yagi K (2007) Impairment of inferior longitudinal fasciculus plays a role in visual memory disturbance. Neurocase 13(2):127–130CrossRefPubMed Shinoura N, Suzuki Y, Tsukada M, Katsuki S, Yamada R, Tabei Y, Saito K, Yagi K (2007) Impairment of inferior longitudinal fasciculus plays a role in visual memory disturbance. Neurocase 13(2):127–130CrossRefPubMed
go back to reference Snow JC, Goodale MA, Culham JC (2015) Preserved haptic shape processing after bilateral LOC lesions. J Neurosci 35(40):13745–13760CrossRefPubMed Snow JC, Goodale MA, Culham JC (2015) Preserved haptic shape processing after bilateral LOC lesions. J Neurosci 35(40):13745–13760CrossRefPubMed
go back to reference Wallraven C, Bülthoff HH, Waterkamp S, van Dam L, Gaißert N (2014) The eyes grasp, the hands see: metric category knowledge transfers between vision and touch. Psychon Bull Rev 21(4):976–985CrossRefPubMed Wallraven C, Bülthoff HH, Waterkamp S, van Dam L, Gaißert N (2014) The eyes grasp, the hands see: metric category knowledge transfers between vision and touch. Psychon Bull Rev 21(4):976–985CrossRefPubMed
go back to reference Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. In: Proceedings of international society for magnetic resonance in medicine Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. In: Proceedings of international society for magnetic resonance in medicine
go back to reference Yendiki A, Koldewyn K, Kakunoori S, Kanwisher N, Fischl B (2014) Spurious group differences due to head motion in a diffusion MRI study. Neuroimage 88:79–90CrossRefPubMed Yendiki A, Koldewyn K, Kakunoori S, Kanwisher N, Fischl B (2014) Spurious group differences due to head motion in a diffusion MRI study. Neuroimage 88:79–90CrossRefPubMed
go back to reference Zhang M, Weisser VD, Stilla R, Prather SC, Sathian K (2004) Multisensory cortical processing of object shape and its relation to mental imagery. Cogn Affect Behav Neurosci 4(2):251–259CrossRefPubMed Zhang M, Weisser VD, Stilla R, Prather SC, Sathian K (2004) Multisensory cortical processing of object shape and its relation to mental imagery. Cogn Affect Behav Neurosci 4(2):251–259CrossRefPubMed
go back to reference Zhang Y, Du A-T, Hayasaka S, G-h Jahng, Hlavin J, Zhan W, Weiner MW, Schuff N (2010) Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis. Neurobiol Aging 31(11):1991–2001CrossRefPubMed Zhang Y, Du A-T, Hayasaka S, G-h Jahng, Hlavin J, Zhan W, Weiner MW, Schuff N (2010) Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis. Neurobiol Aging 31(11):1991–2001CrossRefPubMed
Metadata
Title
Neuroanatomical correlates of haptic object processing: combined evidence from tractography and functional neuroimaging
Authors
Haemy Lee Masson
Hyeok-mook Kang
Laurent Petit
Christian Wallraven
Publication date
01-03-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 2/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1510-3

Other articles of this Issue 2/2018

Brain Structure and Function 2/2018 Go to the issue