The Hitchhiker’s guide to the rhinencephalon

ABSTRACT

Pathology of the rhinencephalon has been a subject of interest in the fields of neurodegenerative diseases, trauma, epilepsy and other neurological conditions. Most of what is known about the human rhinencephalon comes from comparative anatomy studies in other mammals and histological studies in primates. Functional imaging studies can provide new and important insight into the function of the rhinencephalon in humans but have limited spatial resolution, limiting its contribution to the study of the anatomy of the human rhinencephalon. In this study we aim to provide a brief and objective review of the anatomy of this important and often overlooked area of the nervous system.

RESUMO

As patologias do rinencéfalo tem sido assunto de interesse para os estudiosos das doenças neurodegenerativas, do traumatismo cranio-encefálico, epilepsia e outras doenças neurológicas. A maior parte do conhecimento sobre a anatomia do rinencéfalo vem de estudos de anatomia comparativa com outros mamíferos e estudos histológicos em primatas. Estudos de imagem funcional, apesar de proporcionarem informações úteis e interessantes a respeito do funcionamento do rinencéfalo em humanos, sofrem de resolução espacial limitada, e portanto contribuem de maneira restrita ao estudo dos limites das áreas anatçmicas. Neste artigo buscamos proporcionar ao neurologista e neurocientista interessado uma revisão prática e objetiva da anatomia desta área importante e muitas vezes esquecida do sistema nervoso.

olfactory cortex - anatomy - neuroanatomy

córtex olfatório - anatomia - neuroanatomia

Publication History

Received: 02 January 2016

Accepted: 07 January 2016

Article published online:
06 September 2023

• References

• 1 Doty RL. Olfactory dysfunction in Parkinson disease. Nat Rev Neurol. 2012;8(6):329-39. doi:10.1038/nrneurol.2012.80
• 2 Velayudhan L, Gasper A, Pritchard M, Baillon S, Messer C, Proitsi P. Pattern of Smell Identification Impairment in Alzheimer’s Disease. J Alzheimers Dis. 2015;46(2):381-7. doi:10.3233/JAD-142838
• 3 Rupp CI. Olfactory function and schizophrenia: an update. Curr Opin Psychiatry. 2010;23(2):97-102. doi:10.1097/YCO.0b013e328336643f
• 4 Gloor P. The temporal lobe and the limbic system. New York: Oxford University Press; 1997. The olfactory system.
• 5 Paxinos G, Mai J. Atlas of the human brain. 2nd ed. New York: Elsevier Academic Press; 2004.
• 6 Price JL. Olfaction. In: Paxinos, G. editor. The human nervous system. San Diego: Elsevier Academic Press; 2004. p. 1197-211.
• 7 Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991;65(1):175-87. doi:10.1016/0092-8674(91)90418-X
• 8 Buck LB. Unraveling the sense of smell (Nobel lecture). Angew Chem Int Ed Engl. 2005;44(38):6128-40. doi:10.1002/anie.200501120
• 9 Malnic B, Hirono J, Sato T, Buck LB. Combinatorial receptor codes for odors. Cell. 1999;96(5):713-23. doi:10.1016/S0092-8674(00)80581-4
• 10 Eskenazi B, Cain WS, Novelly RA, Friend KB. Olfactory functioning in temporal lobectomy patients. Neuropsychologia. 1983;21(4):365-74. doi:10.1016/0028-3932(83)90023-4
• 11 Eichenbaum H, Morton TH, Potter H, Corkin S. Selective olfactory deficits in case H.M. Brain. 1983;106 (2):459-72. doi:10.1093/brain/106.2.459
• 12 Eskenazi B, Cain WS, Novelly RA, Mattson R. Odor perception in temporal lobe epilepsy patients with and without temporal lobectomy. Neuropsychologia. 1986;24(4):553-62. doi:10.1016/0028-3932(86)90099-0
• 13 Jones-Gotman M, Zatorre RJ. Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia. 1988;26(3):387-400. doi:10.1016/0028-3932(88)90093-0
• 14 Zatorre RJ, Jones-Gotman M. Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain. 1991;114 (1A):71-84.
• 15 Gonçalves Pereira PM, Insausti R, Artacho-Pérula E, Salmenperä T, Kälviäinen R, Pitkänen A. MR volumetric analysis of the piriform cortex and cortical amygdala in drug-refractory temporal lobe epilepsy. AJNR Am J Neuroradiol. 2005;26(2):319-32.
• 16 Gottfried JA, Deichmann R, Winston JS, Dolan RJ. Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci. 2002;22(24):10819-28.
• 17 Zelano C, Bensafi M, Porter J, Mainland J, Johnson B, Bremner E et al. Attentional modulation in human primary olfactory cortex. Nat Neurosci. 2005;8(1):114-20. doi:10.1038/nn1368
• 18 Gottfried JA. A truffle in the mouth is worth two in the bush: odor localization in the human brain. Neuron. 2005;47(4):473-6. doi:10.1016/j.neuron.2005.08.002
• 19 Gottfried JA, Winston JS, Dolan RJ. Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron. 2006;49(3):467-79. doi:10.1016/j.neuron.2006.01.007
• 20 Li W, Luxenberg E, Parrish T, Gottfried JA. Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron. 2006;52(6):1097-108. doi:10.1016/j.neuron.2006.10.026
• 21 Mackay-Sim A. Neurogenesis in the adult olfactory neuroepithelium. In: Doty RL. Handbook of olfaction and gustation. Philadelphia: Marcel Dekker; 2003. p. 93-113.
• 22 Brann JH, Firestein SJ. A lifetime of neurogenesis in the olfactory system. Front Neurosci. 2014;8:182. doi:10.3389/fnins.2014.00182
• 23 Uchida N, Takahashi YK, Tanifuji M, Mori K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci. 2000;3(10):1035-43. doi:10.1038/79857
• 24 Price JL, Russchen FT, Amaral DG. The amygdaloid complex. In: Björklund A, Hökfelt T, Swanson LW. Handbook of chemical neuroanatomy. Amsterdam: Elsevier Science; 1987. p. 279-388.
• 25 Sobel N, Johnson BN, Mainland JD, Yousem DM. Functional neuroimaging of human olfaction. In: Doty RL. Handbook of olfaction and gustation. Philadelphia: Marcel Dekker; 2003.
• 26 Cleland L. Central olfactory structures. In: Doty RL. Handbook of olfaction and gustation. Philadelphia: Marcel Dekker; 2003. p. 165-80.
• 27 Choe HK, Reed MD, Benavidez N, Montgomery D, Soares N, Yim YS et al. Oxytocin Mediates Entrainment of Sensory Stimuli to Social Cues of Opposing Valence. Neuron. 2015;87(1):152-63. doi:10.1016/j.neuron.2015.06.022
• 28 Moran DT, Rowley JC 3rd, Jafek BW, Lovell MA. The fine structure of the olfactory mucosa in man. J Neurocytol. 1982;11(5):721-46. doi:10.1007/BF01153516
• 29 Nakashima T, Kimmelman CP, Snow JB. Structure of human fetal and adult olfactory neuroepithelium. Arch Otolaryngol. 1984;110(10):641-6. doi:10.1001/archotol.1984.00800360013003
• 30 Suzuki Y, Takeda M, Obara N, Suzuki N, Takeichi N. Olfactory epithelium consisting of supporting cells and horizontal basal cells in the posterior nasal cavity of mice. Cell Tissue Res. 2000;299(3):313-25. doi:10.1007/s004410050030
• 31 Doty RL, Kamath V. The influences of age on olfaction: a review. Front Psychol. 2014;5:20. doi:10.3389/fpsyg.2014.00020
• 32 Menco M. Morphology of the mammalian olfactory epithelium: form, fine structure, function and pathology. In: Doty RL. Handbook of olfaction and gustation. Philadelphia: Marcel Dekker; 2003. p. 17-49.
• 33 Jafek BW. Ultrastructure of human nasal mucosa. Laryngoscope. 1983;93(12):1576-99. doi:10.1288/00005537-198312000-00011
• 34 Montani G, Tonelli S, Elsaesser R, Paysan J, Tirindelli R. Neuropeptide Y in the olfactory microvillar cells. Eur J Neurosci. 2006;24(1):20-4. doi:10.1111/j.1460-9568.2006.04878.x
• 35 Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE. Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol. 1998;400(4):469-86. doi:10.1002/(SICI)1096-9861(19981102)400:4<469::AID-CNE3>3.0.CO;2-8
• 36 Beites CL, Kawauchi S, Crocker CE, Calof AL. Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp Cell Res. 2005;306(2):309-16. doi:10.1016/j.yexcr.2005.03.027
• 37 Smith RL, Baker H, Kolstad K, Spencer DD, Greer CA. Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulb. Brain Res. 1991;548(1-2):140-8. doi:10.1016/0006-8993(91)91115-H
• 38 Smith RL, Baker H, Greer CA. Immunohistochemical analyses of the human olfactory bulb. J Comp Neurol. 1993;333(4):519-30. doi:10.1002/cne.903330405
• 39 Kratskin B. Anatomy and neurochemistry of the olfactory bulb. In: Doty RL. Handbook of olfaction and gustation. Philadelphia: Marcel Dekker; 2003. p. 139-64.
• 40 Chen WR, Xiong W, Shepherd GM. Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron. 2000;25(3):625-33. doi:10.1016/S0896-6273(00)81065-X
• 41 Bhatnagar KP, Kennedy RC, Baron G, Greenberg RA. Number of mitral cells and the bulb volume in the aging human olfactory bulb: a quantitative morphological study. Anat Rec. 1987;218(1):73-87. doi:10.1002/ar.1092180112
• 42 Meisami E, Mikhail L, Baim D, Bhatnagar KP. Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann N Y Acad Sci. 1998;855:708-15. doi:10.1111/j.1749-6632.1998.tb10649.x
• 43 Brunjes PC, Illig KR, Meyer EA. A field guide to the anterior olfactory nucleus (cortex). Brain Res Brain Res Rev. 2005;50(2):305-35. doi:10.1016/j.brainresrev.2005.08.005
• 44 Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M et al. A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol. 2001;434(3):289-307. doi:10.1002/cne.1178
• 45 Haberly LB. 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
• 46 Leon M, Johnson B. Functional units in the olfactory system. Proc Natl Acad Sci USA. 2006;103(41):14985-6. doi:10.1073/pnas.0607416103
• 47 Turner BH, Gupta KC, Mishkin M. The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta. J Comp Neurol. 1978;177(3):381-96. doi:10.1002/cne.901770303
• 48 Carmichael ST, Clugnet MC, Price JL. Central olfactory connections in the macaque monkey. J Comp Neurol. 1994;346(3):403-34. doi:10.1002/cne.903460306
• 49 Insausti R, Marcos P, Arroyo-Jiménez MM, Blaizot X, Martínez-Marcos A. Comparative aspects of the olfactory portion of the entorhinal cortex and its projection to the hippocampus in rodents, nonhuman primates, and the human brain. Brain Res Bull. 2002;57(3-4):557-60. doi:10.1016/S0361-9230(01)00684-0
• 50 Allen WF. Distribution of cortical potentials resulting from insufflation of vapors into the nostrils and from stimulation of the olfactory bulbs and the pyriform lobe. Am J Physiol - Leg Content. 1943;139(4):553-5.
• 51 Tanabe T, Iino M, Takagi SF. Discrimination of odors in olfactory bulb, pyriform-amygdaloid areas, and orbitofrontal cortex of the monkey. J Neurophysiol. 1975;38(5):1284-96.
• 52 Tanabe T, Yarita H, Iino M, Ooshima Y, Takagi SF. An olfactory projection area in orbitofrontal cortex of the monkey. J Neurophysiol. 1975;38(5):1269-83.
• 53 Yarita H, Iino M, Tanabe T, Kogure S, Takagi SF. A transthalamic olfactory pathway to orbitofrontal cortex in the monkey. J Neurophysiol. 1980;43(1):69-85.
• 54 Naito J, Kawamura K, Takagi SF. An HRP study of neural pathways to neocortical olfactory areas in monkeys. Neurosci Res. 1984;1(1):19-33. doi:10.1016/0168-0102(84)90027-0
• 55 Zald DH, Pardo JV. Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA. 1997;94(8):4119-24. doi:10.1073/pnas.94.8.4119
• 56 Gottfried JA, Zald DH. On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Brain Res Rev. 2005;50(2):287-304. doi:10.1016/j.brainresrev.2005.08.004
• 57 Bensafi M, Rouby C, Farget V, Bertrand B, Vigouroux M, Holley A. Autonomic nervous system responses to odours: the role of pleasantness and arousal. Chem Senses. 2002;27(8):703-9. doi:10.1093/chemse/27.8.703
• 58 Savic I, Berglund H, Gulyas B, Roland P. Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron. 2001;31(4):661-8. doi:10.1016/S0896-6273(01)00390-7
• 59 Fuller TA, Russchen FT, Price JL. Sources of presumptive glutamergic/aspartergic afferents to the rat ventral striatopallidal region. J Comp Neurol. 1987;258(3):317-38. doi:10.1002/cne.902580302
• 60 Russchen FT, Amaral DG, Price JL. The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol. 1987;256(2):175-210. doi:10.1002/cne.902560202
• 61 Kuroda M, Price JL. Synaptic organization of projections from basal forebrain structures to the mediodorsal thalamic nucleus of the rat. J Comp Neurol. 1991;303(4):513-33. doi:10.1002/cne.903030402
• 62 Kuroda M, Murakami K, Kishi K, Price JL. Distribution of the piriform cortical terminals to cells in the central segment of the mediodorsal thalamic nucleus of the rat. Brain Res. 1992;595(1):159-63. doi:10.1016/0006-8993(92)91468-T