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Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans
Open accessAbstract
Many of the behavioral capacities that distinguish humans from other primates rely on fronto-parietal circuits. The superior longitudinal fasciculus (SLF) is the primary white matter tract connecting lateral frontal with lateral parietal regions; it is distinct from the arcuate fasciculus, which interconnects the frontal and temporal lobes. Here we report a direct, quantitative comparison of SLF connectivity using virtual in vivo dissection of the SLF in chimpanzees and humans. SLF I, the superior-most branch of the SLF, showed similar patterns of connectivity between humans and chimpanzees, and was proportionally volumetrically larger in chimpanzees. SLF II, the middle branch, and SLF III, the inferior-most branch, showed species differences in frontal connectivity. In humans, SLF II showed greater connectivity with dorsolateral prefrontal cortex, whereas in chimps SLF II showed greater connectivity with the inferior frontal gyrus. SLF III was right-lateralized and proportionally volumetrically larger in humans, and human SLF III showed relatively reduced connectivity with dorsal premotor cortex and greater extension into the anterior inferior frontal gyrus, especially in the right hemisphere. These results have implications for the evolution of fronto-parietal functions including spatial attention to observed actions, social learning, and tool use, and are in line with previous research suggesting a unique role for the right anterior inferior frontal gyrus in the evolution of human fronto-parietal network architecture.
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“overall, the right-sided SLF as a whole appears more voluminous than on the left (3, 55).”
From Superior Longitudinal Fasciculus: A Review of the Anatomical Descriptions With Functional Correlates (2022) · cites this paper as [55]
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“whereas the AF is a fronto-temporal tract that passes through the parietal white matter beneath the SLF (55, 56).”
From Superior Longitudinal Fasciculus: A Review of the Anatomical Descriptions With Functional Correlates (2022) · cites this paper as [55]
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“the AF is recognized as a distinctive bundle with connection areas and a trajectory different from that of the SLF”
From Superior Longitudinal Fasciculus: A Review of the Anatomical Descriptions With Functional Correlates (2022) · cites this paper as [55]
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“the SLF is in its essence a fronto-parietal tract, hence connecting the frontal and parietal cortices”
From Superior Longitudinal Fasciculus: A Review of the Anatomical Descriptions With Functional Correlates (2022) · cites this paper as [55]
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Late Acheulean technology and cognition at Boxgrove, UK
Stout, D., Apel, J., Commander, J., & Roberts, M. B. (2013) · Journal of Archaeological Science · doi:10.1016/j.jas.2013.10.001 · Cited by 223 · cited 1×
“By 500,000 years ago, some Acheulean tools exhibited a high level of refinement requiring even more complex production sequences including, for example, the careful preparation of edges and surfaces prior to flake removal (Stout et al., 2014).”
Self-citationLeftward asymmetry in relative fiber density of the arcuate fasciculus
Nucifora, P. G. P., Verma, R., Melhem, E. R., Gur, R. E., & Gur, R. C. (2005) · Neuroreport · doi:10.1097/00001756-200505310-00002 · Cited by 217
Delineation of the middle longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study
Makris, N., Papadimitriou, G. M., Kaiser, J. R., Sorg, S., Kennedy, D. N., & Pandya, D. N. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn124 · Cited by 214
Schenker-Ahmed, N. M., Hopkins, W. D., Spocter, M. A., Garrison, A. R., Stimpson, C. D., Erwin, J. M., Hof, P. R., & Sherwood, C. C. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp138 · Cited by 212 · cited 2×
“There were several extensive cytoarchitectonic studies of the chimpanzee brain several decades ago (Brodmann, 1909; Economo and Parker, 1929; Bailey, 1948; Von Bonin, 1948; Bailey and Von Bonin, 1950; Schenker et al., 2010).”
Chason, J. (1952) · doi:10.1093/ajcp/22.3.272a · Cited by 208
Hartmann, K., Goldenberg, G., Daumüller, M., & Hermsdörfer, J. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.07.015 · Cited by 195
Continuity, Divergence, and the Evolution of Brain Language Pathways
Rilling, J. K., Glasser, M. F., Jbabdi, S., Andersson, J., & Preuss, T. M. (2012) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2011.00011 · Cited by 189 · cited 1×
“, 2007; Glasser and Rilling, 2008) and chimpanzees (Rilling et al., 2011).”
Self-citationHecht, E. E., Gutman, D. A., Khreisheh, N., Taylor, S. V., Kilner, J. M., Faisal, A. A., Bradley, B. A., Chaminade, T., & Stout, D. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0789-6 · Cited by 188
Self-citationHihara, S., Notoya, T., Tanaka, M., Ichinose, S., Ojima, H., Obayashi, S., Fujii, N., & Iriki, A. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2005.11.020 · Cited by 187
“An ape's view of the Oldowan” revisited
Wynn, T., Hernandez‐Aguilar, R. A., Marchant, L. F., & Mcgrew, W. C. (2011) · Evolutionary Anthropology: Issues, News, and Reviews · doi:10.1002/evan.20323 · Cited by 186 · cited 1×
“There is some debate whether these simple “Oldowan” tools represent a departure from shared, “ape-grade” cognitive capacities (Wynn et al., 2011), but their manufacture does require bimanual coordination of accurate, forceful blows that appears difficult or impossible for apes (Byrne, 2005).”
Gray and white matter changes associated with tool-use learning in macaque monkeys
Quallo, M. M., Price, C. J., Ueno, K., Asamizuya, T., Cheng, K., Lemon, R., & Iriki, A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909751106 · Cited by 185
Rizzolatti, G., & Fadiga, L. (2007) · Novartis Foundation symposium · doi:10.1002/9780470515563.ch6 · Cited by 184 · cited 1×
“This network overlaps with an evolutionarily ancient fronto-parietal network for objectdirected grasping (Rizzolatti and Fadiga, 1998) but human tool-use networks are undoubtedly more complex than macaque object-grasping networks.”
Hecht, E. E., Gutman, D. A., Preuss, T. M., Sánchez, M. M., Parr, L. A., & Rilling, J. K. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs097 · Cited by 177
Self-citationTechnology, expertise and social cognition in human evolution
Stout, D., Passingham, R. E., Frith, C., Apel, J., & Chaminade, T. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07619.x · Cited by 168 · cited 2×
“A “mirror-system” or “simulation” account of action understanding suggests that similar neural systems would be involved in the social learning of tool-making methods, and this has been supported by an fMRI study of stone tool-making action observation (Stout et al., 2011).”
Self-citationWhat Puts the How in Where? Tool Use and the Divided Visual Streams Hypothesis
Frey, S. H. (2007) · Cortex · doi:10.1016/s0010-9452(08)70462-3 · Cited by 167 · cited 3×
“It has been proposed that use of “complex” tools (those that alter the functional properties of the hand) requires additional causal understanding resulting from an integration of dorsal (“how”) and ventral (“what”) processing streams in a left-lateralized network of temporal, frontal and parietal areas (Frey, 2007).”
InfluentialVisual neglect in the monkey. Representation and disconnection.
Gaffan, D., & Hornak, J. (1997) · Brain : a journal of neurology · doi:10.1093/brain/120.9.1647 · Cited by 151 · cited 2×
“In monkeys, section of the white matter between the fundus of the intraparietal sulcus and the lateral ventricle produces spatial neglect (Gaffan and Hornak 1997), suggesting a similar role for SLF in spatial attention across macaques, humans and presumably chimpanzees.”
A DTI Investigation of Neural Substrates Supporting Tool Use
Ramayya, A. G., Glasser, M. F., & Rilling, J. K. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp141 · Cited by 151 · cited 1×
“In humans, tool use involves a distributed network of interconnected frontal, parietal, and occipitotemporal regions (Johnson-Frey, 2004; Ramayya et al., 2010; Rilling and Stout, 2014).”
Fuster, J. M. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90204-c · Cited by 140
Prefrontal–parietal function: from foraging to foresight
Genovesio, A., Wise, S. P., & Passingham, R. E. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.11.007 · Cited by 137 · cited 1×
“lineage (Genovesio et al., 2014).”
Modulation of Neural Activity during Observational Learning of Actions and Their Sequential Orders
Frey, S. H., & Gerry, V. E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3914-06.2006 · Cited by 136 · cited 3×
“, 2005) and neuroimaging (Frey and Gerry, 2006; Hamilton and Grafton, 2008) evidence implicate right frontoparietal cortex in the representation of action sequences and goals.”
The human brain: rewired and running hot
Preuss, T. M. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06001.x · Cited by 132 · cited 1×
“More generally, there is evidence for organizational changes and expansion of gray and white matter in the frontal lobes (Smaers et al., 2010; Preuss, 2011; Passingham and Smaers, 2014), changes in frontal and parietal white and gray matter asymmetry (Schenker et al.”
Self-citationStimulus Selectivity in Dorsal and Ventral Prefrontal Cortex after Training in Working Memory Tasks
Meyer, T., Qi, X.-L., Stanford, T. R., & Constantinidis, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6798-10.2011 · Cited by 129
Ten years after: Interference of hospital slack in process performance benefits of quality practices
Goldstein, S., & Iossifova, A. R. (2012) · Journal of Operations Management · doi:10.1016/j.jom.2011.05.003 · Cited by 129
Left inferior parietal cortex integrates time and space during collision judgments.
Assmus, A., Marshall, J., Ritzl, A., Noth, J., Zilles, K., & Fink, G. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.09.025 · Cited by 122
Passingham, R. E., & Smaers, J. B. (2014) · Brain Behavior and Evolution · doi:10.1159/000365183 · Cited by 115
Chen, X., Errangi, B. K., Li, L., Glasser, M. F., Westlye, L. T., Fjell, A. M., Walhovd, K. B., Hu, X. P., Herndon, J. G., Preuss, T. M., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.03.028 · Cited by 114 · cited 1×
“The scans analyzed in the current study were acquired at the Yerkes National Primate Research Center under propofol anesthesia (10 mg/kg/h) using previously described procedures (Chen et al., 2013; Hecht et al., 2013b).”
Self-citationDifferences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans
Hecht, E. E., Murphy, L. E., Gutman, D. A., Votaw, J. R., Schuster, D. M., Preuss, T. M., Orban, G. A., Stout, D., & Parr, L. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2172-13.2013 · Cited by 105
Self-citationThe Mind of the Chimpanzee: Ecological and Experimental Perspectives
Lonsdorf, E., Ross, S., Matsuzawa, T., & Goodall, J. (2010) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226492810.001.0001 · Cited by 104
Schenker, N., Buxhoeveden, D., Blackmon, W., Amunts, K., Zilles, K., & Semendeferi, K. (2008) · The Journal of comparative neurology · doi:10.1002/cne.21792 · Cited by 100
Subcortical anatomy of the lateral association fascicles of the brain: A review
Martino, J., & De Lucas, E. M. (2014) · Clinical Anatomy · doi:10.1002/ca.22321 · Cited by 89
Humans and chimpanzees attend differently to goal-directed actions
Myowa‐Yamakoshi, M., Scola, C., & Hirata, S. (2012) · Nature Communications · doi:10.1038/ncomms1695 · Cited by 87
Smaers, J. B., Schleicher, A., Zilles, K., & Vinicius, L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009123 · Cited by 81 · cited 1×
“More generally, there is evidence for organizational changes and expansion of gray and white matter in the frontal lobes (Smaers et al., 2010; Preuss, 2011; Passingham and Smaers, 2014), changes in frontal and parietal white and gray matter asymmetry (Schenker et al.”
Ventral and dorsal fiber systems for imagined and executed movement
Vry, M., Saur, D., Rijntjes, M., Umarova, R. M., Kellmeyer, P., Schnell, S., Glauche, V., Hamzei, F., & Weiller, C. (2012) · Experimental Brain Research · doi:10.1007/s00221-012-3079-7 · Cited by 81 · cited 1×
“Human SLF II has been implicated in the production of both overt and imagined movements (Vry et al., 2012), as well as in spatial orienting and spatial attention (Suchan et al.”
In vivo architectonics: A cortico-centric perspective
Essen, D. C. V., & Glasser, M. F. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.04.095 · Cited by 62
Serial Organization of Human Behavior in the Inferior Parietal Cortex
Jubault, T., Ody, C., & Koechlin, É. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1986-07.2007 · Cited by 53
Li, L., Preuss, T. M., Rilling, J. K., Hopkins, W. D., Glasser, M. F., Errangi, B. K., Nana, R., Zhang, X., & Hu, X. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012886 · Cited by 53
Self-citationPerisylvian white matter connectivity in the human right hemisphere
Gharabaghi, A., Kunath, F., Erb, M., Saur, R., Heckl, S., Tatagiba, M., Grodd, W., & Karnath, H. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-15 · Cited by 48 · cited 2×
“, 2008), or consider the arcuate to be a subcomponent of the SLF (e.g., Fernandez-Miranda et al., 2008; Gharabaghi et al., 2009; Petrides and Pandya, 2009).”
Fiber pathways connecting cortical areas relevant for spatial orienting and exploration
Suchan, J., Umarova, R. M., Schnell, S., Himmelbach, M., Weiller, C., Karnath, H., & Saur, D. (2013) · Human Brain Mapping · doi:10.1002/hbm.22232 · Cited by 37 · cited 1×
“, 2012), as well as in spatial orienting and spatial attention (Suchan et al., 2014).”
Regional and Hemispheric Variation in Cortical Thickness in Chimpanzees (Pan troglodytes)
Hopkins, W. D., & Avants, B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2996-12.2013 · Cited by 35
Gilissen, E., & Hopkins, W. D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs029 · Cited by 31 · cited 1×
“, 2010; Preuss, 2011; Passingham and Smaers, 2014), changes in frontal and parietal white and gray matter asymmetry (Schenker et al., 2010; Gilissen and Hopkins, 2013; Hopkins and Avants, 2013; Van Essen and Glasser, 2014) and emergence of new functional response properties in inferior frontal (Neubert et al.”
Stout, D. (2013) · The MIT Press eBooks · doi:10.7551/mitpress/9780262019750.003.0009 · Cited by 13 · cited 4×
“Increased human connectivity between the right inferior frontal gyrus and parietal cortex via SLF III may provide an anatomical basis for enhanced cognitive control over the complex goals and multi-step action sequences characteristic of human technology (Stout, 2013).”
InfluentialSelf-citationFunctional organization of monkey brain for abstract operation.
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Evolution of the Human Nervous System Function, Structure, and Development
Sousa, A. M. M., Meyer, K. A., Santpere, G., Gulden, F. O., & Sestan, N. (2017) · Cell · doi:10.1016/j.cell.2017.06.036 · Cited by 517
Brain Lateralization: A Comparative Perspective.
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Warrington, S., Bryant, K. L., Khrapitchev, A., Sallet, J., Charquero-Ballester, M., Douaud, G., Jbabdi, S., Mars, R., & Sotiropoulos, S. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116923 · Cited by 293
“The literature suggests that the SLF2 is right-lateralised, however, fi ndings are less conclusive as in some cases the reported lateralisation does not reach signi fi cance (Hecht et al., 2015; Thiebaut de Schotten et al., 2011a).”
BackgroundResultInfluentialBuilding connectomes using diffusion MRI: why, how and but
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Metadata
- Authors
- Hecht, E. E., Gutman, D. A., Bradley, B. A., Preuss, T. M., & Stout, D.
- Affiliations
- Emory University (US)
- University of Exeter (GB)
- Corresponding author
- Hecht, Erin E.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2015-03
- Volume
- 108
- Pages
- 124-137
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC4324003
- OpenAlex
- W1994212787
- Cited by
- 175
- References
- 127
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 13 · 2023: 13 · 2022: 13 · 2021: 17 · 2020: 44 · 2019: 14 · 2018: 17 · 2017: 13 · 2016: 7 · 2015: 2
- FWCI
- 5.74
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Leverhulme Trust (F/00 144/BP)
- Wenner-Gren Foundation Dissertation Fieldwork Grant and Osmundsen Initiative Award (7699)
- The John Templeton Foundation (40463)
- National Institutes of Health (RR-00165)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- superior longitudinal fasciculus, chimpanzees, human evolution, white matter connectivity, inferior frontal gyrus, dorsolateral prefrontal cortex, dorsal premotor cortex, hemispheric lateralization, arcuate fasciculus, comparative neuroanatomy
- MeSH terms
- Animals, Brain Mapping, Pan troglodytes, Dissection, Biological Evolution, Female, Frontal Lobe, Humans, Image Processing, Computer-Assisted, Male, Neural Pathways, Parietal Lobe, Diffusion Magnetic Resonance Imaging, White Matter
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