Abstract
Through learning and practice, we can acquire numerous skills, ranging from the simple (whistling) to the complex (memorizing operettas in a foreign language). It has been proposed that complex learning requires a network of brain regions that interact with one another via white matter pathways. One candidate white matter pathway, the uncinate fasciculus (UF), has exhibited mixed results for this hypothesis: some studies have shown UF involvement across a range of memory tasks, while other studies report null results. Here, we tested the hypothesis that the UF supports associative memory processes and that this tract can be parcellated into sub-tracts that support specific types of memory. Healthy young adults performed behavioral tasks (two face–name learning tasks, one word pair memory task) and underwent a diffusion-weighted imaging scan. Our results revealed that variation in UF microstructure was significantly associated with individual differences in performance on both face–name tasks, as well as the word association memory task. A UF sub-tract, functionally defined by its connectivity between face-selective regions in the anterior temporal lobe and orbitofrontal cortex, selectively predicted face–name learning. In contrast, connectivity between the fusiform face patch and both anterior face patches had no predictive validity. These findings suggest that there is a robust and replicable relationship between the UF and associative learning and memory. Moreover, this large white matter pathway can be subdivided to reveal discrete functional profiles.
Similar content being viewed by others
References
Alm KH, Rolheiser T, Mohamed FB, Olson IR (2015) Fronto-temporal white matter connectivity predicts reversal learning errors. Front Hum Neurosci 9:1–11. doi:10.3389/fnhum.2015.00343
Alm KH, Rolheiser T, Olson IR (2016) Inter-individual variation in fronto-temporal connectivity predicts the ability to learn different types of associations. Neuroimage 132:213–224. doi:10.1016/j.neuroimage.2016.02.038
Baddeley AD, Emslie H, Nimmo-Smith I (1994) The doors and people test. Thames Valley Test Company, Bury St. Edmunds, UK
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19:2767–2796. doi:10.1093/cercor/bhp055
Browning PGF, Gaffan D (2008) Impairment in object-in-place scene learning after uncinate fascicle section in macaque monkeys. Behav Neurosci 122:477–482. doi:10.1037/0735-7044.122.2.477
Browning PGF, Easton A, Buckley MJ, Gaffan D (2005) The role of prefrontal cortex in object-in-place learning in monkeys. Eur J Neurosci 22:3281–3291. doi:10.1111/j.1460-9568.2005.04477.x
Bussey TJ, Wise SP, Murray EA (2002) Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behav Neurosci 116:703–715. doi:10.1037/0735-7044.116.4.703
Catani M, Dell’Acqua F, Thiebaut de Schotten M (2013) A revised limbic system model for memory, emotion and behaviour. Neurosci Biobehav Rev 37:1724–1737. doi:10.1016/j.neubiorev.2013.07.001
Collins JA, Olson IR (2014) Beyond the FFA: the role of the ventral anterior temporal lobes in face processing. Neuropsychologia 61:65–79. doi:10.1016/j.neuropsychologia.2014.06.005
Conturo TE, Lori NF, Cull TS et al (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci 96:10422–10427. doi:10.1073/PNAS.96.18.10422
Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California verbal learning test, 2nd edn. The Psychological Corporation, San Antonio
Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980. doi:10.1016/j.neuroimage.2006.01.021
Duffau H, Gatignol P, Moritz-Gasser S, Mandonnet E (2009) Is the left uncinate fasciculus essential for language? J Neurol 256:382–389. doi:10.1007/s00415-009-0053-9
Feigl GC, Hiergeist W, Fellner C et al (2014) Magnetic resonance imaging diffusion tensor tractography: evaluation of anatomic accuracy of different fiber tracking software packages. World Neurosurg 81:144–150. doi:10.1016/j.wneu.2013.01.004
Fillard P, Descoteaux M, Goh A et al (2011) Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 56:220–234. doi:10.1016/j.neuroimage.2011.01.032
Frazier JA, Chiu S, Breeze JL et al (2005) Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. Am J Psychiatry 162:1256–1265. doi:10.1176/appi.ajp.162.7.1256
Gaffan D (1992) The role of the hippocampus–fornix–mammillary system in episodic memory, 2nd edn. Guilford Press, New York
Gaffan EA, Gaffan D, Harrison S (1988) Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys. J Neurosci 8:3144–3150
Gainotti G (2013) Laterality effects in normal subjects’ recognition of familiar faces, voices and names. Perceptual and representational components. Neuropsychologia 51:1151–1160. doi:10.1016/j.neuropsychologia.2013.03.009
Goldstein JM, Seidman LJ, Makris N et al (2007) Hypothalamic abnormalities in schizophrenia: sex effects and genetic vulnerability. Biol Psychiatry 61:935–945. doi:10.1016/j.biopsych.2006.06.027
Gomez J, Pestilli F, Witthoft N et al (2015) Functionally defined white matter reveals segregated pathways in human ventral temporal cortex associated with category-specific processing. Neuron 85:216–227. doi:10.1016/j.neuron.2014.12.027
Han Z, Ma Y, Gong G et al (2013) White matter structural connectivity underlying semantic processing: evidence from brain damaged patients. Brain 136:2952–2965. doi:10.1093/brain/awt205
Harvey DY, Wei T, Ellmore TM et al (2013) Neuropsychological evidence for the functional role of the uncinate fasciculus in semantic control. Neuropsychologia 51:789–801. doi:10.1016/j.neuropsychologia.2013.01.028
Hasan KM, Iftikhar A, Kamali A et al (2009) Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography. Brain Res 1276:67–76. doi:10.1016/j.brainres.2009.04.025
Hasan KM, Kamali A, Abid H et al (2010) Quantification of the spatiotemporal microstructural organization of the human brain association, projection and commissural pathways across the lifespan using diffusion tensor tractography. Brain Struct Funct 214:361–373. doi:10.1007/s00429-009-0238-0
Hirni DI, Kivisaari SL, Monsch AU, Taylor KI (2013) Distinct neuroanatomical bases of episodic and semantic memory performance in Alzheimer’s disease. Neuropsychologia 51:930–937. doi:10.1016/j.neuropsychologia.2013.01.013
Huang H, Zhang J, van Zijl PCM, Mori S (2004) Analysis of noise effects on DTI-based tractography using the brute-force and multi-ROI approach. Magn Reson Med 52:559–565. doi:10.1002/mrm.20147
Jenkinson M, Pechaud M, Smith S (2005) BET2-MR-based estimation of brain, skull and scalp surfaces. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), Oxford
Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311. doi:10.1098/Rstb.2006.1934
Kučera H, Francis WN (1967) Computational analysis of present-day American English. Dartmouth Publishing Group, Sudbury
Leirer VO, Morrow DG, Sheikh JI, Pariante GM (1990) Memory skills elders want to improve. Exp Aging Res 16:155–158. doi:10.1080/07340669008251544
Mabbott DJ, Rovet J, Noseworthy MD et al (2009) The relations between white matter and declarative memory in older children and adolescents. Brain Res 1294:80–90. doi:10.1016/j.brainres.2009.07.046
Makris N, Goldstein JM, Kennedy D et al (2006) Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophr Res 83:155–171. doi:10.1016/j.schres.2005.11.020
Markowitsch HJ (1982) Thalamic mediodorsal nucleus and memory: a critical evaluation of studies in animals and man. Neurosci Biobehav Rev 6:351–380. doi:10.1016/0149-7634(82)90046-X
Martin A, Chao LL (2001) Semantic memory and the brain: structure and processes. Curr Opin Neurobiol 11:194–201. doi:10.1016/S0959-4388(00)00196-3
Mehta S, Inoue K, Rudrauf D et al (2016) Segregation of anterior temporal regions critical for retrieving names of unique and non-unique entities reflects underlying long-range connectivity. Cortex 75:1–19. doi:10.1016/j.cortex.2015.10.020
Metzler-Baddeley C, Jones DK, Belaroussi B et al (2011) Frontotemporal connections in episodic memory and aging: a diffusion MRI tractography study. J Neurosci 31:13236–13245. doi:10.1523/JNEUROSCI.2317-11.2011
Mori S, Kaufmann WE, Davatzikos C et al (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47:215–223. doi:10.1002/mrm.10074
Nomura K, Kazui H, Tokunaga H et al (2013) Possible roles of the dominant uncinate fasciculus in naming objects: a case report of intraoperative electrical stimulation on a patient with a brain tumour. Behav Neurol 27:229–234. doi:10.3233/BEN-110249
Nugiel T, Alm KH, Olson IR (2016) Individual differences in white matter microstructure predict semantic control. Cogn Affect Behav Neurosci 16:1003–1016. doi:10.3758/s13415-016-0448-x
Olson IR, Von Der Heide RJ, Alm KH, Vyas G (2015) Development of the uncinate fasciculus: implications for theory and developmental disorders. Dev Cogn Neurosci 14:50–61. doi:10.1016/j.dcn.2015.06.003
Oosterhof NN, Todorov A (2008) The functional basis of face evaluation. Proc Natl Acad Sci 105:11087–11092. doi:10.1073/pnas.0805664105
Papagno C, Miracapillo C, Casarotti A, Romero Lauro LJ, Castellano A, Falini A, Casaceli G, Fava E, Bello L (2011) What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain 134(2):405–414
Papagno C, Casarotti A, Comi A et al (2016) Long-term proper name anomia after removal of the uncinate fasciculus. Brain Struct Funct 221:687–694. doi:10.1007/s00429-014-0920-8
Parker A, Gaffan D (1998) Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions. Neuropsychologia 36:259–271. doi:10.1016/S0028-3932(97)00112-7
Passingham RE, Stephan KE, Kötter R (2002) The anatomical basis of functional localization in the cortex. Nature Rev Neurosci 3(8):606–616
Paternoster R, Brame R, Mazerolle P, Piquero A (1998) Using the correct statistical test for the equality of regression coefficients. Criminology 36:859–866. doi:10.1111/j.1745-9125.1998.tb01268.x
Perrodin C, Kayser C, Abel TJ et al (2015) Who is that? Brain networks and mechanisms for identifying individuals. Trends Cogn Sci 19:783–796. doi:10.1016/j.tics.2015.09.002
Pyles JA, Verstynen TD, Schneider W, Tarr MJ (2013) Explicating the face perception network with white matter connectivity. PLoS One 8:e61611. doi:10.1371/journal.pone.0061611
Rhodes G (1985) Lateralized processes in face recognition. Br J Psychol 76:249–271. doi:10.1111/j.2044-8295.1985.tb01949.x
Rogers TT, Hocking J, Noppeney U et al (2006) Anterior temporal cortex and semantic memory: reconciling findings from neuropsychology and functional imaging. Cogn Affect Behav Neurosci 6:201–213. doi:10.3758/CABN.6.3.201
Sergent J, Signoret J-L, Bruce V, Rolls ET (1992) Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects. Philos Trans R Soc Lond B Biol Sci 335:55–62. doi:10.1098/rstb.1992.0007
Smith SM (2002) Fast robust automated brain extraction. Human Brain Mapp 17(3):143–155
Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219. doi:10.1016/j.neuroimage.2004.07.051
Thomas C, Humphreys K, Jung K-J et al (2011) The anatomy of the callosal and visual-association pathways in high-functioning autism: a DTI tractography study. Cortex 47:863–873. doi:10.1016/j.cortex.2010.07.006
Thomas C, Avram A, Pierpaoli C, Baker C (2015) Diffusion MRI properties of the human uncinate fasciculus correlate with the ability to learn visual associations. Cortex 72:65–78. doi:10.1016/j.cortex.2015.01.023
Troiani V, Dougherty CC, Michael AM, Olson IR (2016) Characterization of face-selective patches in orbitofrontal cortex. Front Hum Neurosci 10:279. doi:10.3389/fnhum.2016.00279
Van Essen DC, Maunsell JHR (1983) Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 6:370–375
Visser M, Embleton KV, Jefferies E et al (2010) The inferior, anterior temporal lobes and semantic memory clarified: novel evidence from distortion-corrected fMRI. Neuropsychologia 48:1689–1696. doi:10.1016/j.neuropsychologia.2010.02.016
Von Der Heide RJ, Skipper LM, Klobusicky E, Olson IR (2013a) Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain 136:1692–1707. doi:10.1093/brain/awt094
Von Der Heide RJ, Skipper LM, Olson IR (2013b) Anterior temporal face patches: a meta-analysis and empirical study. Front Hum Neurosci 7:1–18. doi:10.3389/fnhum.2013.00017
Wakana S, Caprihan A, Panzenboeck MM et al (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36:630–644. doi:10.1016/j.neuroimage.2007.02.049
Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion Toolkit: a software package for diffusion imaging data processing and tractography. Proc Int Soc Mag Reson Med 15:3720
Wechsler D (2009) Wechsler Memory Scale—Fourth Edition (WMS–IV) technical and interpretive manual. Pearson, San Antonio, TX
Zahr NM, Rohlfing T, Pfefferbaum A, Sullivan EV (2009) Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. Neuroimage 44:1050–1062. doi:10.1016/j.neuroimage.2008.09.046
Acknowledgements
We would like to thank William Hampton and Linda Hoffman for assistance with participant testing. This work was supported by a National Institute of Health Grant to I. Olson (RO1 MH091113).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Additional information
The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Metoki, A., Alm, K.H., Wang, Y. et al. Never forget a name: white matter connectivity predicts person memory. Brain Struct Funct 222, 4187–4201 (2017). https://doi.org/10.1007/s00429-017-1458-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-017-1458-3