Role of Ortho-retronasal Olfaction in Mammalian Cortical Evolution

Overview

Journal J Comp Neurol

Specialty Neurology

Date 2015 May 16

PMID 25975561

Citations 23

Authors

Timothy B Rowe

Gordon M Shepherd

Affiliations

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Abstract

Fossils of mammals and their extinct relatives among cynodonts give evidence of correlated transformations affecting olfaction as well as mastication, head movement, and ventilation, and suggest evolutionary coupling of these seemingly separate anatomical regions into a larger integrated system of ortho-retronasal olfaction. Evidence from paleontology and physiology suggests that ortho-retronasal olfaction played a critical role at three stages of mammalian cortical evolution: early mammalian brain development was driven in part by ortho-retronasal olfaction; the bauplan for neocortex had higher-level association functions derived from olfactory cortex; and human cortical evolution was enhanced by ortho-retronasal smell.

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References

Shi P, Zhang J . Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res. 2007; 17(2):166-74. PMC: 1781348. DOI: 10.1101/gr.6040007. View

Heilmann S, Hummel T . A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci. 2004; 118(2):412-9. DOI: 10.1037/0735-7044.118.2.412. View

Niimura Y . Olfactory receptor multigene family in vertebrates: from the viewpoint of evolutionary genomics. Curr Genomics. 2012; 13(2):103-14. PMC: 3308321. DOI: 10.2174/138920212799860706. View

Munoz M, Gaztelu J, GARCIA-AUSTT E . Homo- and heterosynaptic long-term potentiation in the medial cortex of the turtle brain in vitro. Brain Res. 1998; 807(1-2):155-9. DOI: 10.1016/s0006-8993(98)00807-5. View

Grus W, Shi P, Zhang J . Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol Biol Evol. 2007; 24(10):2153-7. DOI: 10.1093/molbev/msm157. View

Shepherd G . Smell images and the flavour system in the human brain. Nature. 2006; 444(7117):316-21. DOI: 10.1038/nature05405. View

HARRISON R . The outgrowth of the nerve fiber as a mode of protoplasmic movement. J Exp Zool. 1959; 142:5-73. DOI: 10.1002/jez.1401420103. View

Shibata M, Gulden F, Sestan N . From trans to cis: transcriptional regulatory networks in neocortical development. Trends Genet. 2015; 31(2):77-87. PMC: 4382006. DOI: 10.1016/j.tig.2014.12.004. View

Luo Z, Chen P, Li G, Chen M . A new eutriconodont mammal and evolutionary development in early mammals. Nature. 2007; 446(7133):288-93. DOI: 10.1038/nature05627. View

10.

Luo Z . Transformation and diversification in early mammal evolution. Nature. 2007; 450(7172):1011-9. DOI: 10.1038/nature06277. View

11.

Harris K, Shepherd G . The neocortical circuit: themes and variations. Nat Neurosci. 2015; 18(2):170-81. PMC: 4889215. DOI: 10.1038/nn.3917. View

12.

Meng J, Hu Y, Wang Y, Wang X, Li C . A Mesozoic gliding mammal from northeastern China. Nature. 2006; 444(7121):889-93. DOI: 10.1038/nature05234. View

13.

Kriegstein A, Connors B . Cellular physiology of the turtle visual cortex: synaptic properties and intrinsic circuitry. J Neurosci. 1986; 6(1):178-91. PMC: 6568623. View

14.

Schlosser G . Making senses development of vertebrate cranial placodes. Int Rev Cell Mol Biol. 2010; 283:129-234. DOI: 10.1016/S1937-6448(10)83004-7. View

15.

Dulac C, Thomas Torello A . Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci. 2003; 4(7):551-62. DOI: 10.1038/nrn1140. View

16.

Haberly L . Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses. 2001; 26(5):551-76. DOI: 10.1093/chemse/26.5.551. View

17.

OLeary M, Bloch J, Flynn J, Gaudin T, Giallombardo A, Giannini N . The placental mammal ancestor and the post-K-Pg radiation of placentals. Science. 2013; 339(6120):662-7. DOI: 10.1126/science.1229237. View

18.

Smith L, Ebner F, COLONNIER M . The thalamocortical projection in Pseudemys turtles: a quantitative electron microscopic study. J Comp Neurol. 1980; 190(3):445-61. DOI: 10.1002/cne.901900304. View

19.

Komiyama T, Luo L . Development of wiring specificity in the olfactory system. Curr Opin Neurobiol. 2005; 16(1):67-73. DOI: 10.1016/j.conb.2005.12.002. View

20.

Sun B, Halpern B . Identification of air phase retronasal and orthonasal odorant pairs. Chem Senses. 2005; 30(8):693-706. DOI: 10.1093/chemse/bji062. View