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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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“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).”
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“The other finding has to do with the volume of the bundles; overall, the right-sided SLF as a whole appears more voluminous than on the left (3, 55).”
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“Chimpanzees again appear intermediate, with a weak but observable extension of SLFIII into vlPFC and no evidence of right-lateralization at the population level (87).”
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“Seed and anterior target placement was guided by a previous DTI study on chimpanzee SLF anatomy [5].”
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“Thus, to make the least number of assumptions is to rely on the relative sizes of tracts within species to anchor our analysis, as in previous comparative Diffusion Tensor Imaging (DTI) work (102).”
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BackgroundManrique, H. M., Friston, K. J., & WALKER, M. J. (2024) · Physics of Life Reviews · doi:10.1016/j.plrev.2024.01.004 · Cited by 24
“…to knap ‘handaxes ’ shows changes in superior longitudinal fasciculus white matter between frontal, parietal, temporal, and occipital cortices [122,143,144,145], with impingements, that plausibly facilitate rapid attentional switching, on ventrolateral prefrontal cortices, the right inferior…”
BackgroundMargiotoudi, K., Bohn, M., Schwob, N., Taglialatela, J., Pulvermüller, F., Epping, A. J., Schweller, K., & Allritz, M. (2022) · Proceedings of the Royal Society B · doi:10.1098/rspb.2021.1717 · Cited by 18
“Specifically, long white matter cortical connections between frontal and posterior temporal cortices, such as the arcuate fasciculus [45,46] or the superior longitudinal fasciculus [47] are not as strongly developed in great apes.”
Measurement of Sylvian Fissure asymmetry and occipital bending in humans and Pan troglodytes
Hou, L., Xiang, L., Crow, T. J., Leroy, F., Rivière, D., Mangin, J. F., & Roberts, N. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.08.045 · Cited by 18
“In parallel with our findings in the SF, the underlying white matter fibre tracts are reported not to be lateralised in chimpanzees (Rilling et al., 2008; Hecht et al., 2015), raising the possibility that surface asymmetries in humans may be related to lateralised white matter changes.”
BackgroundInvestigation of superior longitudinal fasciculus fiber complexity in recent onset psychosis
Szeszko, P. R., Tan, E. T., Uluğ, A. M., Kingsley, P. B., Gallego, J. A., Rhindress, K., Malhotra, A. K., Robinson, D. G., & Marinelli, L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.10.019 · Cited by 19
“In addition, studies investigating the comparative neuroanatomy of the SLF implicate a unique role for this white-matter bundle in the evolution of human fronto parietal networks associated with action imitation and concomitant social learning (Hecht et al., 2015) with other evidence suggesting that self-recognition f…”
BackgroundÇini, N., Pennisi, M., Genç, S., Spandidos, D. A., Falzone, L., Mitsias, P., Tsatsakis, A., & Taghizadehghalehjoughi, A. (2024) · Oncology Report · doi:10.3892/or.2024.8798 · Cited by 17
“However, some studies in the literature are not concordant indicating that SLF is greater on the right side than on the left side (47,51), while other studies have claimed that SLF II is dominant on the left side through multiple components (49,52).”
ResultBauer, C. M., & Merabet, L. B. (2024) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2301001 · Cited by 18
“End points were in the caudal middle frontal, lateral orbitofrontal, medial orbitofrontal, pars opercularis, pars orbitalis, pars triangularis, rostral middle frontal, and superior frontal regions [15,16,35–38].”
In vivo mapping of the deep and superficial white matter connectivity in the chimpanzee brain
Chauvel, M., Uszynski, I., Herlin, B., Popov, A., Leprince, Y., Mangin, J., Hopkins, W. D., & Poupon, C. (2023) · bioRxiv · doi:10.1016/j.neuroimage.2023.120362 · Cited by 14
The uniqueness of the human brain: a review
Pittella, J. E. H. (2024) · Dementia & Neuropsychologia · doi:10.1590/1980-5764-dn-2023-0078 · Cited by 15
“In humans, as compared to chimpanzees, there is greater connectivity of the superior longitudinal fasciculus with the lateral frontal cortex (dorsolateral prefrontal cortex and inferior frontal gyrus), more to the right in the latter, thus evidencing lateralization 73 .”
BackgroundXia, X., Fan, L., Chen, C., Yao, R., Deng, H., Zhao, D., Li, H., & Jiang, T. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00623 · Cited by 10
“, 2008, 2011) along with many other white matter fibers (Zhang et al., 2013; Hecht et al., 2015).”
BackgroundMethodIndividual variation in the chimpanzee arcuate fasciculus predicts vocal and gestural communication
Hecht, E. E., Vijayakumar, S., Becker, Y., & Hopkins, W. D. (2025) · Nature Communications · doi:10.1038/s41467-025-58784-5 · Cited by 12
“The frontaland parietalgraymatter masks are equivalent to those used in prior studies 70,71 .”
Self-citationAnatomical organization of forebrain circuits in the primate
Giarrocco, F., & Averbeck, B. B. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02586-8 · Cited by 21
“Stronger prefrontal connectivity of the vSLF, along with its right lateralization, has been suggested to reflect higher cognitive functions and human motor skills such as the use of tools and social learning (Hecht et al. 2015; Thiebaut de Schotten et al. 2012).”
BackgroundImproving innovative decision-making: Training-induced changes in fronto-parietal networks
Crespi, C., Martinez, D. L., Dodich, A., Cappa, S. F., Brusoni, S., Zollo, M., Falini, A., & Canessa, N. (2018) · Brain and Cognition · doi:10.1016/j.bandc.2018.11.004 · Cited by 16
“The superior longitudinal fasciculus is a long-range bidirectional bundle connecting frontal and parietal regions (Thiebaut de Schotten et al., 2012; Hecht et al., 2015), involved in several functions ranging from eye movements and visuospatial processing to sensory-motor integration and…”
BackgroundArchaeology and the evolutionary neuroscience of language
Stout, D. (2018) · Interaction Studies Social Behaviour and Communication in Biological and Artificial Systems · doi:10.1075/is.17033.sto · Cited by 17
Self-citationLiang, W., Yu, Q., Wang, W., Dhollander, T., Suluba, E., Li, Z., Xu, F., Hu, Y., Tang, Y., & Liu, S. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02565-z · Cited by 14
Bhoyroo, R., Hands, B. P., Caeyenberghs, K., Luca, A. D., Leemans, A., Wigley, A., & Hyde, C. E. (2021) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617721001168 · Cited by 11
Electrodermal activity during Lower Paleolithic stone tool handling
Fedato, A., Silva‐Gago, M., Bernal, M. T., Alcalde, R. A., Guerra, E. M., & Bruner, E. (2019) · American Journal of Human Biology · doi:10.1002/ajhb.23279 · Cited by 17
Eichert, N., Robinson, E. C., Bryant, K., Jbabdi, S., Jenkinson, M., Li, L., Krug, K., Watkins, K. E., & Mars, R. B. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/645234 · Cited by 7
“, 2018c; Schmahmann and Pandya, 2009) and the chimpanzee SLF3 and AF are similar to previous reports (Hecht et al., 2015; Rilling et al., 2008).”
InfluentialHegarty, C. E., Jolles, D., Mennigen, E., Jalbrzikowski, M., Bearden, C., & Karlsgodt, K. (2018) · bioRxiv · doi:10.1101/423574 · Cited by 10
“We used a predefined ROI that predominantly includes the frontoparietal portion [traditionally, SLF I, II, and III (85)] without extensive temporoparietal connections.”
MethodThe Evolution of Mammalian Brains from Early Mammals to Present-Day Primates
Kaas, J. H. (2017) · Springer eBooks · doi:10.1007/978-4-431-56559-8_3 · Cited by 15
A map of white matter tracts in a lesser ape, the lar gibbon
Bryant, K. L., Manger, P., Bertelsen, M. F., Khrapitchev, A., Sallet, J., Benn, R. A., & Mars, R. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02709-9 · Cited by 8
Putt, S. S., Anwarzai, Z., Holden, C., Ruck, L., & Schoenemann, P. T. (2022) · International Journal of Primatology · doi:10.1007/s10764-021-00267-7 · Cited by 12
“…as well as regions in the junction between the temporal and parietal lobes (particularly near AG, SMG, and posterior MTG), as well as the underlying white matter pathways that connect these brain areas (Glasser & Rilling, 2008; Hecht et al., 2015; Schoenemann, 2006, 2018; Smaers et al., 2017).”
Aykan, S., Puglia, M. H., Kalaycıoğlu, C., Pelphrey, K. A., Tunçalı, T., & Nalçacı, E. (2021) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-021-04924-x · Cited by 9
Neurodiversity as a Conceptual Lens and Topic of Cross-Cultural Study
Cascio, M. A. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374.027 · Cited by 7
Boch, M., Karl, S., Wagner, I. C., Lengersdorff, L., Huber, L., & Lamm, C. (2024) · Imaging Neuroscience · doi:10.1162/imag_a_00385 · Cited by 14
“…are densely interconnected and play a crucial role in sensory and visuomotor integration during action observation and execution ( Glover et al., 2012; Hecht et al., 2015; Hecht, Gutman, et al., 2013), one might hypothesize that the absence of parietal and premotor activation in dogs may be linked.”
Anatomical bases of fast parietal grasp control in humans: A diffusion-MRI tractography study
Richard, N., Desmurget, M., Teillac, A., Beuriat, P.-A., Bardi, L., Coudé, G., Szathmári, A., Mottolèse, C., Sirigu, A., & Hiba, B. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118002 · Cited by 9
“This is much more than he percentages found for SLF-III (22”
InfluentialRitual and Religion as Social Technologies of Cooperation
Kavanagh, C. M., Jong, J., & Whitehouse, H. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374.016 · Cited by 7
Neuroanthropological Perspectives on Culture, Mind, and Brain
Lende, D. H., & Downey, G. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374.014 · Cited by 10
Kirmayer, L. J., Worthman, C. M., & Kitayama, S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374.028 · Cited by 8
Computational challenges of evolving the language-ready brain
Arbib, M. (2018) · Benjamins Current Topics · doi:10.1075/is.17036.arb · Cited by 5
Preuss, T. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-420190-3.00008-9 · Cited by 17
Self-citationInsights From Language‐Trained Apes: Brain Network Plasticity and Communication
Erbaba, B., Sinha, M., Guevara, E. E., Hecht, E. E., Hopkins, W. D., & Sherwood, C. C. (2025) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.70018 · Cited by 2
Self-citationConversion of concept-specific decision confidence into integrative introspection in primates
Miyamoto, K., Setsuie, R., & Miyashita, Y. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110581 · Cited by 5
Mutual Constitution of Culture and the Mind
Kitayama, S., & Yu, Q. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374.006 · Cited by 9
(2020) · Cambridge University Press eBooks · doi:10.1017/9781108695374 · Cited by 30
Xia, X., Fan, L., Chen, C., Cheng, L., Cao, L., He, B., Chen, J., Li, H., & Jiang, T. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.12.147546 · Cited by 4
“…al., 2015; Cloutman and Lambon Ralph, 2012) and has been used to describe species differences in specific fiber pathways (Rilling et al., 2011; Zhang et al., 2013; Hecht et al. 2015; Folloni et al., 2019) and whole-brain connectivity profiles (Mars et al., 2016, 2018a, 2018b; Neubert et al., 2015).”
MethodIntelligence in Multiple Dimensions: Evolutionary Framework for the Study of Human Cognition
Geary, D. C. (2026) · Intelligence & Cognitive Abilities · doi:10.65550/001c.154815 · Cited by 3
Brosse, S., Tremblay, C., Mérida, I., & Frasnelli, J. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1503841 · Cited by 3
Deferm, W., Tang, T., Moerkerke, M., Daniëls, N., Steyaert, J. G., Alaerts, K., Ortibus, E., Naulaers, G., & Boets, B. (2024) · NeuroImage Clinical · doi:10.1016/j.nicl.2024.103580 · Cited by 4
“There is neuroanatomical evidence that both the SLF II and SLF III may play a role in social learning but in a different manner (Hecht et al., 2015).”
BackgroundCadaveric White Matter Dissection Study of the Telencephalic Flexure: Surgical Implications
González-López, P., Cossu, G., Thomas, C., Marston, J. S., Gómez, C., Pralong, E., Messerer, M., & Daniel, R. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.757757 · Cited by 3
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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