Semantic representation in the white matter pathway

PLoS Biol. 2018 Apr 6;16(4):e2003993. doi: 10.1371/journal.pbio.2003993. eCollection 2018 Apr.

Abstract

Object conceptual processing has been localized to distributed cortical regions that represent specific attributes. A challenging question is how object semantic space is formed. We tested a novel framework of representing semantic space in the pattern of white matter (WM) connections by extending the representational similarity analysis (RSA) to structural lesion pattern and behavioral data in 80 brain-damaged patients. For each WM connection, a neural representational dissimilarity matrix (RDM) was computed by first building machine-learning models with the voxel-wise WM lesion patterns as features to predict naming performance of a particular item and then computing the correlation between the predicted naming score and the actual naming score of another item in the testing patients. This correlation was used to build the neural RDM based on the assumption that if the connection pattern contains certain aspects of information shared by the naming processes of these two items, models trained with one item should also predict naming accuracy of the other. Correlating the neural RDM with various cognitive RDMs revealed that neural patterns in several WM connections that connect left occipital/middle temporal regions and anterior temporal regions associated with the object semantic space. Such associations were not attributable to modality-specific attributes (shape, manipulation, color, and motion), to peripheral picture-naming processes (picture visual similarity, phonological similarity), to broad semantic categories, or to the properties of the cortical regions that they connected, which tended to represent multiple modality-specific attributes. That is, the semantic space could be represented through WM connection patterns across cortical regions representing modality-specific attributes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Brain Damage, Chronic / diagnostic imaging
  • Brain Damage, Chronic / pathology
  • Brain Damage, Chronic / physiopathology*
  • Case-Control Studies
  • Female
  • Humans
  • Machine Learning
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Nerve Net / anatomy & histology
  • Nerve Net / diagnostic imaging
  • Nerve Net / physiology*
  • Neuropsychological Tests
  • Occipital Lobe / anatomy & histology
  • Occipital Lobe / diagnostic imaging
  • Occipital Lobe / physiology*
  • Pattern Recognition, Visual / physiology*
  • Semantics*
  • Temporal Lobe / anatomy & histology
  • Temporal Lobe / diagnostic imaging
  • Temporal Lobe / physiology*
  • White Matter / anatomy & histology
  • White Matter / diagnostic imaging
  • White Matter / physiology*

Grants and funding

National Key Basic Research Program of China www.most.gov.cn (grant number 2013CB837300, 2014CB846100). Received by YB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Beijing Brain Project www.bjkw.gov.cn (grant number Z16110100020000, Z161100000216125). Received by YB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Natural Science Foundation of China www.nsfc.gov.cn (grant number 4131671128, 31521063, 81671772, 31700944). 4131671128, 31521063 received by YB; 81671772 received by GG; 31700944 received by YF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Program for Special Support of Top-notch Young Professionals. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.