The white matter structural network underlying human tool use and tool understanding.
The ability to recognize, create, and use complex tools is a milestone in human evolution. Widely distributed brain regions in parietal, frontal, and temporal cortices have been implicated in using and understanding tools, but the roles of their anatomical connections in supporting tool use and tool conceptual behaviors are unclear. Using deterministic fiber tracking in healthy participants, we first examined how 14 cortical regions that are consistently activated by tool processing are connected by white matter (WM) tracts. The relationship between the integrity of each of the 33 obtained tracts and tool processing deficits across 86 brain-damaged patients was investigated. WM tract integrity was measured with both lesion percentage (structural imaging) and mean fractional anisotropy (FA) values (diffusion imaging). Behavioral abilities were assessed by a tool use task, a range of conceptual tasks, and control tasks. We found that three left hemisphere tracts connecting frontoparietal and intrafrontal areas overlapping with left superior longitudinal fasciculus are crucial for tool use such that larger lesion and lower mean FA values on these tracts were associated with more severe tool use deficits. These tracts and five additional left hemisphere tracts connecting frontal and temporal/parietal regions, mainly overlapping with left superior longitudinal fasciculus, inferior frontooccipital fasciculus, uncinate fasciculus, and anterior thalamic radiation, are crucial for tool concept processing. Largely consistent results were also obtained using voxel-based symptom mapping analyses. Our results revealed the WM structural networks that support the use and conceptual understanding of tools, providing evidence for the anatomical skeleton of the tool knowledge network.
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Yanchao
Y
Bi
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China, zzhhan@bnu.edu.cn.
Zaizhu
Z
Han
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Suyu
S
Zhong
Department of Psychology, Henan University, Kaifeng 475000, China.
Yujun
Y
Ma
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Gaolang
G
Gong
Center for the Study of Applied Psychology, Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, School of Psychology, South China Normal University, Guangzhou 510631, China.
Ruiwang
R
Huang
Neurorehabilitation Department of Capital Medical University Rehabilitation College and China Rehabilitation Research Center, Beijing 100038, China.
Luping
L
Song
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Yuxing
Y
Fang
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Yong
Y
He
Department of Psychology, Harvard University, Cambridge, Massachusetts 02138, and Center of Mind/Brain Sciences (CIMeC), University of Trento, I-38122 Trento, Italy.
Alfonso
A
Caramazza
D000328:Adult; D000368:Aged; D016880:Anisotropy; D001930:Brain Injuries / Q000150:complications / Q000473:pathology; D001931:Brain Mapping; D003072:Cognition Disorders / Q000209:etiology / Q000473:pathology; D032882:Comprehension; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008297:Male; D008875:Middle Aged; D019957:Motor Skills Disorders / Q000209:etiology / Q000473:pathology; D009415:Nerve Net / Q000502:physiology*; D009483:Neuropsychological Tests; D015203:Reproducibility of Results; D053001:Tool Use Behavior / Q000502:physiology*; D066127:White Matter / Q000473:pathology* / Q000502:physiology
brain-damaged patient; diffusion tensor imaging; structural network; tool concept; tool use; voxel-based lesion-symptom mapping