Hostname: page-component-7b9c58cd5d-dlb68 Total loading time: 0 Render date: 2025-03-15T00:33:33.418Z Has data issue: false hasContentIssue false
  • English
  • Français

Variation in White Matter Connectivity Predicts the Ability to Remember Faces and Discriminate Their Emotions

Published online by Cambridge University Press:  18 February 2016

Ashley Unger ,
Kylie H. Alm ,
Jessica A. Collins ,
Jacquelyn M. O’Leary  and
Ingrid R. Olson
Ashley Unger
Affiliation:
Temple University, Department of Psychology, Philadelphia, Pennsylvania
Kylie H. Alm
Affiliation:
Temple University, Department of Psychology, Philadelphia, Pennsylvania
Jessica A. Collins
Affiliation:
Massachusetts General Hospital, Department of Neurology, Boston, Massachusetts
Jacquelyn M. O’Leary
Affiliation:
Temple University, Department of Psychology, Philadelphia, Pennsylvania
Ingrid R. Olson*
Affiliation:
Temple University, Department of Psychology, Philadelphia, Pennsylvania
*
Correspondence and reprint requests to: Ingrid R. Olson, Temple University, Weiss Hall, 1701 N. 13th Street, Philadelphia, PA 19122. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: The extended face network contains clusters of neurons that perform distinct functions on facial stimuli. Regions in the posterior ventral visual stream appear to perform basic perceptual functions on faces, while more anterior regions, such as the ventral anterior temporal lobe and amygdala, function to link mnemonic and affective information to faces. Anterior and posterior regions are interconnected by a long-range white matter tracts; however, it is not known if variation in connectivity of these pathways explains cognitive performance. Methods: Here, we used diffusion imaging and deterministic tractography in a cohort of 28 neurologically normal adults ages 18–28 to examine microstructural properties of visual fiber pathways and their relationship to certain mnemonic and affective functions involved in face processing. We investigated how inter-individual variability in two tracts, the inferior longitudinal fasciculus (ILF) and the inferior fronto-occipital fasciculus (IFOF), related to performance on tests of facial emotion recognition and face memory. Results: Results revealed that microstructure of both tracts predicted variability in behavioral performance indexed by both tasks, suggesting that the ILF and IFOF play a role in facilitating our ability to discriminate emotional expressions in faces, as well as to remember unique faces. Variation in a control tract, the uncinate fasciculus, did not predict performance on these tasks. Conclusions: These results corroborate and extend the findings of previous neuropsychology studies investigating the effects of damage to the ILF and IFOF, and demonstrate that differences in face processing abilities are related to white matter microstructure, even in healthy individuals. (JINS, 2016, 22, 180–190)

Keywords

Diffusion imagingFacesEmotionProsopagnosiaFace memoryHypoemotionality
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Supplement 2: Human Brain Connectivity in the Modern Era: Relevance to Understanding Health and Disease , February 2016 , pp. 180 - 190
Copyright
Copyright © The International Neuropsychological Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, A.L., Hurley, S.A., Samsonov, A.A., Adluru, N., Hosseinbor, A.P., Mossahebi, P., & Field, A.S. (2011). Characterization of cerebral white matter properties using quantitative magnetic resonance imaging stains. Brain Connectivity, 1(6), 423–446. http://doi.org/10.1089/brain.2011.0071 Google Scholar
Alexander, A.L., Lee, J.E., Lazar, M., & Field, A.S. (2007b). Diffusion tensor imaging of the brain. Neurotherapeutics, 4(3), 316–329. http://doi.org/10.1016/j.nurt.2007.05.011 Google Scholar
Alm, K.H., Rolheiser, T., Mohamed, F.B., & Olson, I.R. (2015). Fronto-temporal white matter connectivity predicts reversal learning errors. Frontiers in Neuroscience, 9(343), 1–11. doi:10.3389/fnhum.2015.00343 Google ScholarPubMed
Almairac, F., Herbet, G., Moritz-Gasser, S., de Champfleur, N.M., & Duffau, H. (2014). The left inferior fronto-occipital fasciculus subserves language semantics: A multilevel lesion study. Brain Structure & Function. http://doi.org/10.1007/s00429-014-0773-1 Google Scholar
Baggio, H.C., Segura, B., Ibarretxe-Bilbao, N., Valldeoriola, F., Marti, M.J., Compta, Y., & Junqué, C. (2012). Structural correlates of facial emotion recognition deficits in Parkinson’s disease patients. Neuropsychologia, 50(8), 2121–2128. http://doi.org/10.1016/j.neuropsychologia.2012.05.020 Google Scholar
Bauer, R.M. (1982). Visual hypoemotionality as a symptom of visual-limbic disconnection in man. Archives of Neurology, 39(11), 702–708. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7126000 CrossRefGoogle ScholarPubMed
Braem, B., Honoré, J., Rousseaux, M., Saj, A., & Coello, Y. (2014). Integration of visual and haptic informations in the perception of the vertical in young and old healthy adults and right brain-damaged patients. Neurophysiologie Clinique, 44(1), 41–48. http://doi.org/10.1016/j.neucli.2013.10.137 Google Scholar
Catani, M. (2007). From hodology to function. Brain, 130(Pt 3), 602–605. http://doi.org/10.1093/brain/awm008 Google Scholar
Catani, M., Jones, D.K., Donato, R., & Ffytche, D.H. (2003). Occipito-temporal connections in the human brain. Brain, 126(Pt 9), 2093–2107. http://doi.org/10.1093/brain/awg203 CrossRefGoogle ScholarPubMed
Catani, M., & Thiebaut de Schotten, M. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex, 44(8), 1105–1132. http://doi.org/10.1016/j.cortex.2008.05.004 Google Scholar
Coello, A.F., 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. Journal of Neurosurgery, 118(1), 202–205. http://doi.org/10.3171/2012.10.JNS12527 Google Scholar
Coello, Y., Bartolo, A., Amiri, B., Devanne, H., Houdayer, E., & Derambure, P. (2008). Perceiving what is reachable depends on motor representations: Evidence from a transcranial magnetic stimulation study. PLoS One, 3(8), e2862. http://doi.org/10.1371/journal.pone.0002862 CrossRefGoogle ScholarPubMed
De Zubicaray, G.I., Rose, S.E., & McMahon, K.L. (2011). The structure and connectivity of semantic memory in the healthy older adult brain. Neuroimage, 54(2), 1488–1494. http://doi.org/10.1016/j.neuroimage.2010.08.058 Google Scholar
Diehl, B., Busch, R.M., Duncan, J.S., Piao, Z., Tkach, J., & Lüders, H.O. (2008). Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia, 49(8), 1409–1418. http://doi.org/10.1111/j.1528-1167.2008.01596.x Google Scholar
Duchaine, B., & Nakayama, K. (2006). The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia, 44(4), 576–585. http://doi.org/10.1016/j.neuropsychologia.2005.07.001 Google Scholar
Duffau, H., Gatignol, P., Mandonnet, E., Peruzzi, P., Tzourio-Mazoyer, N., & Capelle, L. (2005). New insights into the anatomo-functional connectivity of the semantic system: A study using cortico-subcortical electrostimulations. Brain, 128(Pt 4), 797–810. http://doi.org/10.1093/brain/awh423 CrossRefGoogle ScholarPubMed
Duffau, H., Peggy Gatignol, S.T., Mandonnet, E., Capelle, L., & Taillandier, L. (2008). Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. Journal of Neurosurgery, 109(3), 461–471. http://doi.org/10.3171/JNS/2008/109/9/0461 Google Scholar
Ekman, P., & Friesen, W.V. (1976). Measuring facial movement. Environmental Psychology and Nonverbal Behavior, 1(1), 56–75. http://doi.org/10.1007/BF01115465 Google Scholar
Epelbaum, S., Pinel, P., Gaillard, R., Delmaire, C., Perrin, M., Dupont, S., & Cohen, L. (2008). Pure alexia as a disconnection syndrome: New diffusion imaging evidence for an old concept. Cortex, 44(8), 962–974. http://doi.org/10.1016/j.cortex.2008.05.003 CrossRefGoogle ScholarPubMed
Genova, H.M., Rajagopalan, V., Chiaravalloti, N., Binder, A., Deluca, J., & Lengenfelder, J. (2015). Facial affect recognition linked to damage in specific white matter tracts in traumatic brain injury. Social Neuroscience, 10(1), 27–34. doi:10.1080/17470919.2014.959618.Google Scholar
Gil-Robles, S., Carvallo, A., Jimenez, M.D.M., Gomez Caicoya, A., Martinez, R., Ruiz-Ocaña, C., & Duffau, H. (2013). Double dissociation between visual recognition and picture naming: A study of the visual language connectivity using tractography and brain stimulation. Neurosurgery, 72(4), 678–686. http://doi.org/10.1227/NEU.0b013e318282a361 Google Scholar
Gong, G., He, Y., & Evans, A.C. (2011). Brain connectivity: Gender makes a difference. The Neuroscientist, 17(5), 575–591. http://doi.org/10.1177/1073858410386492 CrossRefGoogle ScholarPubMed
Grossi, D., Soricelli, A., Ponari, M., Salvatore, E., Quarantelli, M., Prinster, A., & Trojano, L. (2014). Structural connectivity in a single case of progressive prosopagnosia: The role of the right inferior longitudinal fasciculus. Cortex, 56, 111–120. http://doi.org/10.1016/j.cortex.2012.09.010 Google Scholar
Habib, M. (1986). Visual hypoemotionality and prosopagnosia associated with right temporal lobe isolation. Neuropsychologia, 24(4), 577–582. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/3774141 CrossRefGoogle ScholarPubMed
Hoeft, F., Meyler, A., Hernandez, A., Juel, C., Taylor-Hill, H., Martindale, J.L., McMillon, G., Kolchugina, G., … Gabrieli, J. D. (2007). Functional and morphometric brain dissociation between dyslexia and reading ability. Behavioral Neuroscience, 121(3), 602–613.Google Scholar
Horel, J.A., & Misantone, L.J. (1974). The Klüver-Bucy syndrome produced by partial isolation of the temporal lobe. Experimental Neurology, 42(1), 101–112. http://doi.org/10.1016/0014-4886(74)90010-7 Google Scholar
Ingalhalikar, M., Smith, A., Parker, D., Satterthwaite, T.D., Elliott, M.A., Ruparel, K., & Verma, R. (2014). Sex differences in the structural connectome of the human brain. Proceedings of the National Academy of Sciences of the United States of America, 111(2), 823–828. http://doi.org/10.1073/pnas.1316909110 Google Scholar
Johansen-Berg, H., & Behrens, T.E.J. (2009). Diffusion MRI. Amsterdam: Elsevier. http://doi.org/10.1016/B978-0-12-374709-9.00022-5 Google Scholar
Jones, D.K. (2008). Studying connections in the living human brain with diffusion MRI. Cortex, 44(8), 936–952. http://doi.org/10.1016/j.cortex.2008.05.002 Google Scholar
Lebel, C., Gee, M., Camicioli, R., Wieler, M., Martin, W., & Beaulieu, C. (2012). Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage, 60(1), 340–352. http://doi.org/10.1016/j.neuroimage.2011.11.094 CrossRefGoogle ScholarPubMed
Mandonnet, E., Nouet, A., Gatignol, P., Capelle, L., & Duffau, H. (2007). Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain, 130(Pt 3), 623–629. http://doi.org/10.1093/brain/awl361 Google Scholar
McDonald, C.R., Hagler, D.J., Girard, H.M., Pung, C., Ahmadi, M.E., Holland, D., & Dale, A.M. (2010). Changes in fiber tract integrity and visual fields after anterior temporal lobectomy. Neurology, 75(18), 1631–1638. http://doi.org/10.1212/WNL.0b013e3181fb44db Google Scholar
Metzler-Baddeley, C., Jones, D.K., Belaroussi, B., Aggleton, J.P., & O’Sullivan, M.J. (2011). Frontotemporal connections in episodic memory and aging: A diffusion MRI tractography study. The Journal of Neuroscience, 31(37), 13236–13245. http://doi.org/10.1523/JNEUROSCI.2317-11.2011 Google Scholar
Mori, S., Crain, B.J., Chacko, V.P., & Van Zijl, P.C.M. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology, 45(2), 265–269. http://doi.org/10.1002/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3 Google Scholar
Mori, S., Kaufmann, W.E., Davatzikos, C., Stieltjes, B., Amodei, L., Fredericksen, K., & van Zijl, P.C.M. (2002). Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magnetic Resonance in Medicine, 47(2), 215–223. http://doi.org/10.1002/mrm.10074 Google Scholar
Mundfrom, D.J., Piccone, A., Perrett, J.J., Schaffer, J., & Roozeboom, M. (2006). Bonferroni adjustments in tests for regression coefficients. Multiple Linear Regression Viewpoints, 32, 1–6.Google Scholar
Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C.E., Kolster, R., Lee, H., & McCandliss, B.D. (2008). Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain, 131(Pt 12), 3209–3221. http://doi.org/10.1093/brain/awn247 Google Scholar
Olson, I.R., Heide, R.J., Alm, K.H., & Vyas, G. (2015). Development of the uncinate fasciculus: implications for theory and developmental disorders. Developmental Cognitive Neuroscience, 14, 50–61.Google Scholar
Philippi, C.L., Mehta, S., Grabowski, T., Adolphs, R., & Rudrauf, D. (2009). Damage to association fiber tracts impairs recognition of the facial expression of emotion. The Journal of Neuroscience, 29(48), 15089–15099. http://doi.org/10.1523/JNEUROSCI.0796-09.2009 Google Scholar
Sarubbo, S., De Benedictis, A., Maldonado, I.L., Basso, G., & Duffau, H. (2013). Frontal terminations for the inferior fronto-occipital fascicle: Anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Structure & Function, 218(1), 21–37. http://doi.org/10.1007/s00429-011-0372-3 Google Scholar
Schmahmann, J.D., & Pandya, D.N. (2007). The complex history of the fronto-occipital fasciculus. Journal of the History of the Neurosciences, 16, 362–377.CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E.J., Johansen-Berg, H., & Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl. 1), S208–S219. http://doi.org/10.1016/j.neuroimage.2004.07.051 Google Scholar
Sprague, J.M. (1966). Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science (New York, N.Y.), 153(3743), 1544–1547. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/5917786 Google Scholar
Tavor, I., Yablonski, M., Mezer, A., Rom, S., Assaf, Y., & Yovel, G. (2014). Separate parts of occipito-temporal white matter fibers are associated with recognition of faces and places. Neuroimage, 86(2014), 123–130. http://doi.org/10.1016/j.neuroimage.2013.07.085 Google Scholar
Thomas, A.L., Lawler, K., Olson, I.R., & Aguirre, G.K. (2008). The Philadelphia Face Perception Battery. Archives of Clinical Neuropsychology, 23(2), 175–187. http://doi.org/10.1016/j.acn.2007.10.003 Google Scholar
Thomas, C., Avidan, G., Humphreys, K., Jung, K., Gao, F., & Behrmann, M. (2009). Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia. Nature Neuroscience, 12(1), 29–31. http://doi.org/10.1038/nn.2224 CrossRefGoogle ScholarPubMed
Thomas, C., Humphreys, K., Jung, K.-J., Minshew, N., & Behrmann, M. (2010). The anatomy of the callosal and visual-association pathways in high-functioning autism: A DTI tractography study. Cortex, 47(7), 863–873. http://doi.org/10.1016/j.cortex.2010.07.006 Google Scholar
Thomas, C., Moya, L., Avidan, G., Humphreys, K., Jung, K.J., Peterson, M.A., & Behrmann, M. (2008). Reduction in white matter connectivity, revealed by diffusion tensor imaging, may account for age-related changes in face perception. Journal of Cognitive Neuroscience, 20(2), 268–284.Google Scholar
Tournier, J.-D., Mori, S., & Leemans, A. (2011). Diffusion tensor imaging and beyond. Magnetic Resonance in Medicine, 65(6), 1532–1556. http://doi.org/10.1002/mrm.22924 Google Scholar
Valdés-Sosa, M., Bobes, M.A., Quiñones, I., Garcia, L., Valdes-Hernandez, P.A., Iturria, Y., & Asencio, J. (2011). Covert face recognition without the fusiform-temporal pathways. Neuroimage, 57(3), 1162–1176. http://doi.org/10.1016/j.neuroimage.2011.04.057 Google Scholar
Von Der Heide, R.J., Skipper, L.M., Klobusicky, E., & Olson, I.R. (2013). Dissecting the uncinate fasciculus: Disorders, controversies and a hypothesis. Brain, 136(Pt 6), 1692–1707. http://doi.org/10.1093/brain/awt094 Google Scholar
Wakana, S., Caprihan, A., Panzenboeck, M.M., Fallon, J.H., Perry, M., Gollub, R.L., & Mori, S. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage, 36(3), 630–644. http://doi.org/10.1016/j.neuroimage.2007.02.049 CrossRefGoogle ScholarPubMed
Wang, R., Benner, T., Sorensen, A.G., & Wedeen, V.J. (2007). Diffusion toolkit: A software package for diffusion imaging data processing and tractography. Proceedings of the 15th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, Seattle, Washington. Abstract 3720.Google Scholar
Yamasaki, T., Taniwaki, T., Tobimatsu, S., Arakawa, K., Kuba, H., Maeda, Y., & Kira, J. (2004). Electrophysiological correlates of associative visual agnosia lesioned in the ventral pathway. Journal of the Neurological Sciences, 221(1-2), 53–60. http://doi.org/10.1016/j.jns.2004.03.024 Google Scholar
Yeatman, J.D., Rauschecker, A.M., & Wandell, B.A. (2013). Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections. Brain and Language, 125(2), 146–155. http://doi.org/10.1016/j.bandl.2012.04.010 Google Scholar
Zemmoura, I., Herbet, G., Moritz-Gasser, S., & Duffau, H. (2015). New insights into the neural network mediating reading processes provided by cortico-subcortical electrical mapping. Human Brain Mapping, 36, 2215–2230. http://doi.org/10.1002/hbm.22766 Google Scholar
Supplementary material: File

Unger supplementary material

Tables S1-S3

Download Unger supplementary material(File)
File 23.4 KB