Anchoring the human olfactory system to a functional gradient
https://doi.org/10.1101/2020.03.19.998849Abstract
ABSTRACTMargulies et al. (2016) demonstrated the existence of at least five independent functional connectivity gradients in the human brain. However, it is unclear how these functional gradients might link to anatomy. The dual origin theory proposes that differences in cortical cytoarchitecture originate from two trends of progressive differentiation between the different layers of the cortex, referred to as the hippocampocentric and olfactocentric systems. When conceptualising the functional connectivity gradients within the evolutionary framework of the Dual Origin theory, the first gradient likely represents the hippocampocentric system anatomically. Here we expand on this concept and demonstrate that the fifth gradient likely links to the olfactocentric system. We describe the anatomy of the latter as well as the evidence to support this hypothesis. Together, the first and fifth gradients might help to model the Dual Origin theory of the human brain and inform brain models and ...
References (39)
- Abbie, A.A., 1940. Cortical lamination in the monotremata. J Comp Neurol 72, 429-467.
- Abbie, A.A., 1942. Cortical lamination in a polyprotodont marsupial, Perameles nasuta. J Comp Neurol 76, 509-536.
- Aboitiz, F., Montiel, J.F., 2015. Olfaction, navigation, and the origin of isocortex. Front Neurosci 9, 402.
- Alves, P.N., Foulon, C., Karolis, V., Bzdok, D., Margulies, D.S., Volle, E., Thiebaut de Schotten, M., 2019. An improved neuroanatomical model of the default-mode network reconciles previous neuroimaging and neuropathological findings. Commun Biol 2, 370.
- Arnold, T.C., You, Y., Ding, M., Zuo, X.-N., de Araujo, I., Li, W., 2019. Functional connectome analyses reveal a highly optimized human olfactory network. bioRxiv, 843532.
- Blazquez Freches, G., Haak, K., Bryant, K., Schurz, M., Beckmann, C., Mars, R., in press. Principles of temporal association cortex organisation as revealed by connectivity gradients. Brain Structure and Function.
- 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.
- Chiou, R., Lambon Ralph, M.A., 2016. The anterior temporal cortex is a primary semantic source of top-down influences on object recognition. Cortex 79, 75-86.
- Chu, S., Downes, J.J., 2002. Proust nose best: odors are better cues of autobiographical memory. Mem Cognit 30, 511-518.
- Coifman, R.R., Lafon, S., Lee, A.B., Maggioni, M., Nadler, B., Warner, F., Zucker, S.W., 2005. Geometric diffusions as a tool for harmonic analysis and structure definition of data: diffusion maps. Proc Natl Acad Sci U S A 102, 7426-7431.
- Corbetta, M., Shulman, G.L., 2002. Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience 3, 201-215.
- Corkin, S., 2013. Permanent Present Tense: The Unforgettable Life of the Amnesic Patient H.M. Basic Books, Philadelphia.
- Dart, R.A., 1934. The Dual Structure of the Neopallium: its History and Significance. J Anat 69, 3-19.
- Glasser, M.F., Smith, S.M., Marcus, D.S., Andersson, J.L., Auerbach, E.J., Behrens, T.E., Coalson, T.S., Harms, M.P., Jenkinson, M., Moeller, S., Robinson, E.C., Sotiropoulos, S.N., Xu, J., Yacoub, E., Ugurbil, K., Van Essen, D.C., 2016. The Human Connectome Project's neuroimaging approach. Nat Neurosci 19, 1175-1187.
- Hebb, D.O., 1949. The Organization of Behavior: A Neuropsychological Theory. Wiley and Sons, New York.
- Herz, R.S., Cupchik, G.C., 1995. The emotional distinctiveness of odor-evoked memories. Chem Senses 20, 517-528.
- Honey, C.J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J.P., Meuli, R., Hagmann, P., 2009. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A 106, 2035-2040.
- Jacobs, L.F., 2012. From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci U S A 109 Suppl 1, 10693-10700.
- Louail, M., Gilissen, E., Prat, S., Garcia, C., Bouret, S., 2019. Refining the ecological brain: Strong relation between the ventromedial prefrontal cortex and feeding ecology in five primate species. Cortex 118, 262-274.
- Margulies, D.S., Ghosh, S.S., Goulas, A., Falkiewicz, M., Huntenburg, J.M., Langs, G., Bezgin, G., Eickhoff, S.B., Castellanos, F.X., Petrides, M., Jefferies, E., Smallwood, J., 2016. Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci U S A 113, 12574-12579.
- Mars, R.B., Sotiropoulos, S.N., Passingham, R.E., Sallet, J., Verhagen, L., Khrapitchev, A.A., Sibson, N., Jbabdi, S., 2018. Whole brain comparative anatomy using connectivity blueprints. Elife 7.
- Mars, R.B., Verhagen, L., Gladwin, T.E., Neubert, F.X., Sallet, J., Rushworth, M.F., 2016. Comparing brains by matching connectivity profiles. Neurosci Biobehav Rev 60, 90-97.
- Mesulam, M.M., Thompson, C.K., Weintraub, S., Rogalski, E.J., 2015. The Wernicke conundrum and the anatomy of language comprehension in primary progressive aphasia. Brain 138, 2423-2437.
- Milham, M.P., Ai, L., Koo, B., Xu, T., Amiez, C., Balezeau, F., Baxter, M.G., Blezer, E.L.A., Brochier, T., Chen, A., Croxson, P.L., Damatac, C.G., Dehaene, S., Everling, S., Fair, D.A., Fleysher, L., Freiwald, W., Froudist-Walsh, S., Griffiths, T.D., Guedj, C., Hadj-Bouziane, F., Ben Hamed, S., Harel, N., Hiba, B., Jarraya, B., Jung, B., Kastner, S., Klink, P.C., Kwok, S.C., Laland, K.N., Leopold, D.A., Lindenfors, P., Mars, R.B., Menon, R.S., Messinger, A., Meunier, M., Mok, K., Morrison, J.H., Nacef, J., Nagy, J., Rios, M.O., Petkov, C.I., Pinsk, M., Poirier, C., Procyk, E., Rajimehr, R., Reader, S.M., Roelfsema, P.R., Rudko, D.A., Rushworth, M.F.S., Russ, B.E., Sallet, J., Schmid, M.C., Schwiedrzik, C.M., Seidlitz, J., Sein, J., Shmuel, A., Sullivan, E.L., Ungerleider, L., Thiele, A., Todorov, O.S., Tsao, D., Wang, Z., Wilson, C.R.E., Yacoub, E., Ye, F.Q., Zarco, W., Zhou, Y.D., Margulies, D.S., Schroeder, C.E., 2018. An Open Resource for Non-human Primate Imaging. Neuron 100, 61-74 e62.
- Milton, K., 1981. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. American Anthropologist 83, 534-548.
- Ogawa, S., Lee, T.M., Kay, A.R., Tank, D.W., 1990. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 87, 9868-9872.
- Olman, C.A., Davachi, L., Inati, S., 2009. Distortion and signal loss in medial temporal lobe. PLoS One 4, e8160.
- Pandya, D.N., Petrides, M., Cipolloni, P., 2017. Cerebral cortex: architecture, connections, and the dual origin concept. Oxford University Press, New York.
- Pandya, D.N., Yeterian, E.H., 1990. Architecture and connections of cerebral cortex: Implications for brain evolution and function. The Guilfor Press, New York, NY.
- Purves, D., Williams, S.M., 2001. Neuroscience, 2nd ed. Sinauer Associates, Sunderland, Mass.
- Reep, R.L., Finlay, B.L., Darlington, R.B., 2007. The limbic system in Mammalian brain evolution. Brain Behav Evol 70, 57-70.
- Royet, J.P., Hudry, J., Zald, D.H., Godinot, D., Gregoire, M.C., Lavenne, F., Costes, N., Holley, A., 2001. Functional neuroanatomy of different olfactory judgments. Neuroimage 13, 506-519.
- Sanides, F., 1962. Die Architektonik des menschlichen Stirnhirns; zugleich eine Darstellung der Prinzipien seiner Gestaltung als Spiegel der stammesgeschichtlichen Differenzierung der Grosshirnrinde. [Architectonics of the human frontal lobe of the brain. With a demonstration of the principles of its formation as a reflection of phylogenetic differentiation of the cerebral cortex.] Monogr Gesamtgeb Neurol Psychiatr. 98, 1-201.
- Sanides, F., 1964. The cyto-myeloarchitecture of the human frontal lobe and its relation to phylogenetic differentiation of the cerebral cortex. J. Hirnforsch 6, 269-282.
- Savic, I., Gulyas, B., Larsson, M., Roland, P., 2000. Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26, 735-745.
- Spearman, C., 1904. The proof and measurement of association between two things. Am J Psychol 15, 441-471.
- Thiebaut de Schotten, M., Croxson, P.L., Mars, R.B., 2019. Large-scale comparative neuroimaging: Where are we and what do we need? Cortex 118, 188-202.
- Willander, J., Larsson, M., 2006. Smell your way back to childhood: autobiographical odor memory. Psychon Bull Rev 13, 240-244.
- Workshop, P.R.D.E.G.C., Consortium. Electronic address, m.m.c.o., Workshop, P.R.D.E.G.C., Consortium, 2020. Accelerating the Evolution of Nonhuman Primate Neuroimaging. Neuron 105, 600-603.