Vùng vỏ não trước trán của cừu. Đặc điểm địa hình, tổ chức, hóa sinh thần kinh, hình ảnh tensor số và so sánh với tinh tinh và con người

Brain Structure and Function - Tập 227 - Trang 1871-1891 - 2022
Tommaso Gerussi1, Jean-Marie Graïc1, Annamaria Grandis2, Antonella Peruffo1, Bruno Cozzi1
1Department of Comparative Biomedicine and Food Science (BCA), University of Padova, Legnaro, Italy
2Department of Veterinary Medical Sciences, University of Bologna, Ozzano dell’Emilia, Italy

Tóm tắt

Các vùng dành riêng cho chức năng não bộ cao hơn như vỏ não trước trán (OFC) được cho là đặc trưng riêng cho họ Hominidae. Vùng OFC tham gia vào hành vi xã hội, mã hóa phần thưởng và hình phạt cũng như kiểm soát cảm xúc. Ở đây, chúng tôi tập trung vào vùng tương ứng có thể có ở cừu để đánh giá tính đồng nhất của nó so với OFC ở con người. Chúng tôi đã sử dụng phương pháp mô học cổ điển trên năm con cừu (Ovis aries) và bốn con tinh tinh (Pan troglodytes) như một loài linh trưởng có vỏ não sáu lớp, và hình ảnh Tensor Khuếch tán (DTI) trên ba con cừu và năm bộ não người. Nhuộm Nissl cho thấy sự biến đổi nhất định trong việc phân lớp vỏ não khi không tìm thấy lớp IV ở cừu. Sự giảm tổng độ dày vỏ não cũng được thể hiện rõ, đi kèm với sự giảm tỷ lệ của lớp một và sự gia tăng của lớp hai trên tổng độ dày. Phép theo dõi đường dẫn thần kinh của OFC cừu, ngược lại, đã tiết lộ những điểm tương đồng với các đường dẫn ở người và những đường đã được mô tả trong tài liệu, cùng với một số lượng cao hơn của sợi cortico-cortical kết nối OFC với các vùng thị giác ở bán cầu phải. Kết quả của chúng tôi cho thấy sự hiện diện của các thành phần cơ bản cần thiết cho tư duy trừu tượng phức tạp ở cừu và sự tính bên rõ rệt, thường liên quan đến hiệu quả cao hơn của một chức năng nhất định, cho thấy sự thích nghi tiến hóa của loài con mồi này.

Từ khóa

#vỏ não trước trán #cừu #tinh tinh #hình ảnh tensor khuếch tán #tư duy trừu tượng #tiến hóa

Tài liệu tham khảo

Alves NT, Fukusima SS, Aznar-Casanova JA (2008) Models of brain asymmetry in emotional processing. Psychol Neurosci 1:63–66. https://doi.org/10.3922/j.psns.2008.1.010 Bailey P, Bonin GV, McCulloch WS (1950) The isocortex of the chimpanzee. Univ. Illinois Press Barone R, Bortolami R (2004) Anatomie comparée des mammifères domestiques: tome 6, neurologie I, système nerveux central. Editions Vigot, Paris Baynes K (2002) Corpus callosum. In: Ramachandran VS (ed) Encyclopedia of the human brain. Academic Press, pp 51–64 Brodmann K (1905) Beiträge zur histologischen Lokalisation der Grosshirnrinde. III. Mitteilung: Die Rindenfelder der niederen Affen. J Psychol Neurol 4:177–226 Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth, Leipzig Cameron OG (2001) Visceral sensory neuroscience: interoception. Oxford University Press Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346:403–434. https://doi.org/10.1002/cne.903460306 Chincarini M, Dalla Costa E, Qiu L et al (2020) Reliability of fNIRS for noninvasive monitoring of brain function and emotion in sheep. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-71704-5 Conner AK, Briggs RG, Sali G et al (2018) A connectomic atlas of the human cerebrum—chapter 13: tractographic description of the inferior fronto-occipital fasciculus. Operative Neurosurg 15(suppl_1):S436–S443. https://doi.org/10.1093/ons/opy267 Constantinescu GM (2018) Illustrated veterinary anatomical nomenclature. Thieme, Stuttgard, Germany Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly by thalamus. Science 340:1591–1594. https://doi.org/10.1126/science.1236425 Cozzi B, De Giorgio A, Peruffo A et al (2017) The laminar organization of the motor cortex in monodactylous mammals: a comparative assessment based on horse, chimpanzee, and macaque. Brain Struct Funct 222:2743–2757. https://doi.org/10.1007/s00429-017-1369-3 Cozzi B, Bonfanti L, Canali E, Minero M (2020) Brain waste: the neglect of animal brains. Front Neuroanat 14:573934. https://doi.org/10.3389/fnana.2020.573934 Da Costa AP, Leigh AE, Man MS, Kendrick KM (2004) Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep. P Roy Soc B-Biol Sci 271:2077–2084. https://doi.org/10.1098/rspb.2004.2831 D’Arceuil H, de Crespigny A (2007) The effects of brain tissue decomposition on diffusion tensor imaging and tractography. NeuroIm 36(1):64–68. https://doi.org/10.1016/j.neuroimage.2007.02.039 DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1–19. https://doi.org/10.1016/s0891-0618(97)10013-8 Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53:1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010 Dinopoulos A, Karamanlidis AN, Papadopoulos G, Antonopoulos J, Michaloudi H (1985) Thalamic projections to motor, prefrontal, and somatosensory cortex in the sheep studied by means of the horseradish peroxidase retrograde transport method. J Comp Neurol 241:63–81. https://doi.org/10.1002/cne.902410106 Ella A, Delgadillo JA, Chemineau P, Keller M (2017) Computation of a high resolution MRI 3D stereotaxic atlas of the sheep brain. J Comp Neurol 525(3):676–692 Fernández-Miranda JC, Rhoton AL, Kakizawa Y, Choi C, Álvarez-Linera J (2008) The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg 108:764–774. https://doi.org/10.3171/JNS/2008/108/4/0764 Fuster JM (1997) The prefrontal cortex. Raven Press, New York Fuster JM (2015) The prefrontal cortex. Academic Press, London Glezer II, Hof PR, Leranth C, Morgane PJ (1993) Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cereb Cortex 3:249–272. https://doi.org/10.1093/cercor/3.3.249 Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC (2016) The heritability of chimpanzee and human brain asymmetry. Proc R Soc B: Biol Sci 283(1845):20161319 Graïc JM, Peruffo A, Corain L, Centelleghe C, Granato A, Zanellato E, Cozzi B (2020) Asymmetry in the cytoarchitecture of the area 44 homolog of the brain of the chimpanzee Pan troglodytes. Front Neuroanat 14:55. https://doi.org/10.3389/fnana.2020.00055 Graïc JM, Peruffo A, Grandis A, Cozzi B (2021a) Topographical and structural characterization of the V1–V2 transition zone in the visual cortex of the long-finned pilot whale Globicephala melas (Traill, 1809). Anat Rec 304:1105–1118. https://doi.org/10.1002/ar.24558 Graïc JM, Peruffo A, Corain L et al (2021b) The primary visual cortex of Cetartiodactyls: organization, cytoarchitectonics and comparison with perissodactyls and primates. Brain Struct Funct. https://doi.org/10.1007/s00429-021-02392-8 Gu J, Gu X (2003) Induced gene expression in human brain after the split from chimpanzee. Trends Genet 19(2):63–65 Guigere M, Goldman-Rakic PS (1988) Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkey. J Comp Neurol 277:195–213. https://doi.org/10.1002/cne.902770204 Guillamón ML, Clau LB (2010) The sheep as a large animal experimental model in respiratory diseases research. Arch Bronconeumol 46:499–501. https://doi.org/10.1016/j.arbres.2010.06.005 Guldimann K, Vögeli S, Wolf M, Wechsler B, Gygax L (2015) Frontal brain deactivation during a non-verbal cognitive judgement bias test in sheep. Brain Cognition 93:35–41. https://doi.org/10.1016/j.bandc.2014.11.004 Güntürkün O, Ströckens F, Ocklenburg S (2020) Brain lateralization: a comparative perspective. Physiol Rev 100:1019–1063. https://doi.org/10.1152/physrev.00006.2019 Gygax L, Voegeli S (2016) Reactions of sheep towards three sets of emotional stimuli: (In) consistency in respect to stimulus valence and sheep identity. Appl Anim Behav Sci 174:51–57. https://doi.org/10.1016/j.applanim.2015.11.015 Gygax L, Reefmann N, Wolf M, Langbein J (2013) Prefrontal cortex activity, sympatho-vagal reaction and behaviour distinguish between situations of feed reward and frustration in dwarf goats. Behav Brain Res 239:104–114. https://doi.org/10.1016/j.bbr.2012.10.052 Hau J, Sarubbo S, Houde JC et al (2017) Revisiting the human uncinate fasciculus, its subcomponents and asymmetries with stem-based tractography and microdissection validation. Brain Struct Funct 222:1645–1662. https://doi.org/10.1007/s00429-016-1298-6 Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287:1153–1163. https://doi.org/10.1002/ar.a.2025 Hof PR, Mufson EJ, Morrison JH (1995) Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation. J Comp Neurol 359:48–68. https://doi.org/10.1002/cne.903590105 Hof PR, Glezer II, Flagg RA (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77–116. https://doi.org/10.1016/S0891-0618(98)00065-9 Hof PR, Glezer II, Nimchinsky EA, Erwin JM (2000) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav Evol 55:300–310. https://doi.org/10.1159/000006665 Jacobsen JC, Bawden CS, Rudiger SR et al (2010) An ovine transgenic Huntington’s disease model. Hum Mol Genet 19:1873–1882. https://doi.org/10.1093/hmg/ddq063 Jelsing J, Hay-Schmidt A, Dyrby T et al (2006) The prefrontal cortex in the Göttingen minipig brain defined by neural projection criteria and cytoarchitecture. Brain Res Bull 70:322–336. https://doi.org/10.1016/j.brainresbull.2006.06.009 Jeurissen B, Descoteaux M, Mori S, Leemans A (2019) Diffusion MRI fiber tractography of the brain. NMR Biomed 32:e3785. https://doi.org/10.1002/nbm.3785 Kendrick KM, da Costa AP, Leigh AE, Hinton MR, Peirce JW (2001) Sheep don’t forget a face. Nature 414:165–166. https://doi.org/10.1038/35102669 Kier EL, Staib LH, Davis LM, Bronen RA (2004) MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. Am J Neuroradiol 25:677–691 Knolle F, Goncalves RP, Morton AJ (2017) Sheep recognize familiar and unfamiliar human faces from two-dimensional images. R Soc Open Sci 4:171228. https://doi.org/10.1098/rsos.171228 Kringelbach M, Rolls A (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 72:341–372. https://doi.org/10.1016/j.pneurobio.2004.03.006 La Rosa C, Cavallo F, Pecora A et al (2020) Phylogenetic variation in cortical layer II immature neuron reservoir of mammals. Elife 9:e55456. https://doi.org/10.7554/eLife.55456 Leliveld LM, Langbein J, Puppe B (2013) The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Appl Anim Behav Sci 145:1–14. https://doi.org/10.1016/j.applanim.2013.02.002 Liu J, Liu B, Zhang X, Yu B, Guan W, Wang K, Yang Y, Gong Y, Wu X, Yanagawa Y, Wu S, Zhao C (2014) Calretinin-positive L5a pyramidal neurons in the development of the paralemniscal pathway in the barrel cortex. Mol Brain 7:84. https://doi.org/10.1186/s13041-014-0084-8 Lopez-Persem A, Roumazeilles L, Folloni D (2020) Differential functional connectivity underlying asymmetric reward-related activity in human and nonhuman primates. P Natl Acad Sci USA 117:28452–28462. https://doi.org/10.1073/pnas.2000759117 Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379(1):113–132 Meurisse M, Chaillou E, Lévy F (2009) Afferent and efferent connections of the cortical and medial nuclei of the amygdala in sheep. J Chem Neuroanat 37:87–97. https://doi.org/10.1016/j.jchemneu.2008.09.001 Min HK, Hwang SC, Marsh, MP et al (2012) Deep brain stimulation induces BOLD activation in motor and non-motor networks: an fMRI comparison study of STN and EN/GPi DBS in large animals. Neuroimage 63:1408–1420. https://doi.org/10.1016/j.neuroimage.2012.08.006 Morton AJ, Howland DS (2013) Large genetic animal models of Huntington’s disease. J Huntingt Dis 2:3–19. https://doi.org/10.3233/JHD-130050 Mtui E, Gruener G, Dockery P (2020) Fitzgerald’s clinical neuroanatomy and neuroscience, 7th edn. Elsevier O’Doherty J, Kringelback ML, Rolls ET, Hornak J, Andrew C (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4:95–102. https://doi.org/10.1038/82959 Öngür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219. https://doi.org/10.1093/cercor/10.3.206 Ono M, Kubik S, Abernathy CD (1990) Atlas of the cerebral sulci. Georg Thieme Verlag, Stuttgart Peirce JW, Kendrick KM (2002) Functional asymmetry in sheep temporal cortex. NeuroReport 13:2395–2399. https://doi.org/10.1097/00001756-200212200-00004 Peirce JW, Leigh AE, Kendrick KM (2000) Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia 38:475–483. https://doi.org/10.1016/S0028-3932(99)00088-3 Peirce JW, Leigh AE, Kendrick KM (2001) Human face recognition in sheep: lack of configurational coding and right hemisphere advantage. Behav Process 55:13–26. https://doi.org/10.1016/S0376-6357(01)00158-9 Peruffo A, Corain L, Bombardi C et al (2019) The motor cortex of the sheep: laminar organization, projections and diffusion tensor imaging of the intracranial pyramidal and extrapyramidal tracts. Brain Struc Funct 224:1933–1946. https://doi.org/10.1007/s00429-019-01885-x Petrides M, Pandya DN (1994) Comparative cytoarchitectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amsterdam, pp 17–58 Petrides M, Pandya DN (2012) The frontal cortex. In: Mai J, Paxinos G (eds) The human nervous system. Academic Press, pp 988–1011 Rane S, Duong TQ (2011) Comparison of in vivo and ex vivo diffusion tensor imaging in rhesus macaques at short and long diffusion times. Open Neuroimaging J 5:172–178. https://doi.org/10.2174/1874440001105010172 Ray JP, Price JL (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337:1–31. https://doi.org/10.1002/cne.903370102 Rempel-Clower NL, Barbas H (1998) Topographic organization of connections between the hypothalamus and prefrontal cortex in the rhesus monkey. J Comp Neurol 398:393–419. https://doi.org/10.1002/(SICI)1096-9861(19980831)398:3%3c393::AID-CNE7%3e3.0.CO;2-V Rose JE (1942) A cytoarchitectural study of the sheep cortex. J Comp Neurol 76:1–55. https://doi.org/10.1002/cne.900760102 Rose JE, Woolsey CN (1948) The orbitofrontal cortex and its connections with the mediodorsal nucleus in rabbit, sheep and cat. Res Publ Assoc Res Nerv Ment Dis 27:210–232 (PMID: 18106857) Rudebeck PH, Rich EL (2018) Orbitofrontal cortex. Curr Biol 28:1083–1088. https://doi.org/10.1016/j.cub.2018.07.018 Saper CB (2012) Hypothalamus. In: Mai J, Paxinos G (eds) The human nervous system. Academic Press, pp 548–583 Sartoretto SC, Uzeda MJ, Miguel FB, Nascimento JR, Ascoli F, Calasans-Maia MD (2016) Sheep as an experimental model for biomaterial implant evaluation. Acta Ortop Bras 24:262–266. https://doi.org/10.1590/1413-785220162405161949 Schilling KG, Petit L, Rheault F et al (2020) Brain connections derived from diffusion MRI tractography can be highly anatomically accurate—if we know where white matter pathways start, where they end, and where they do not go. Brain Struct Funct 225:2387–2402. https://doi.org/10.1007/s00429-020-02129-z Tranel D, Cooper G, Rodnitzky RL (2003) Higher brain functions. Neuroscience in medicine. Humana Press, Totowa, NJ, pp 621–639 van Eden CG, Uylings HBM (1985) Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol 241:253–267. https://doi.org/10.1002/cne.902410302 Versace E, Morgante M, Pulina G, Vallortigara G (2007) Behavioural lateralization in sheep (Ovis aries). Behav Brain Res 184:72–80. https://doi.org/10.1016/j.bbr.2007.06.016 Vögeli S, Lutz J, Wolf M, Wechsler B, Gygax L (2014) Valence of physical stimuli, not housing conditions, affects behaviour and frontal cortical brain activity in sheep. Behav Brain Res 267:144–155. https://doi.org/10.1016/j.bbr.2014.03.036 Vögeli S, Wolf M, Wechsler B, Gygax L (2015) Frontal brain activity and behavioral indicators of affective states are weakly affected by thermal stimuli in sheep living in different housing conditions. Front Vet Sci 2:9. https://doi.org/10.3389/fvets.2015.00009 Walker AE (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73:59–86. https://doi.org/10.1002/cne.900730106 Wang C, Song L, Zhang R et al (2018) Impact of fixation, coil, and number of excitations on diffusion tensor imaging of rat brains at 7.0 T. Eur Radiol Exp 2:25. https://doi.org/10.1186/s41747-018-0057-2 Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31(3):1116–28