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Evolutionary Formation and Functional Significance of the Core–Belt Pattern of Neural Organization of Rostral Auditory Centers in Vertebrates

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Abstract

We survey the literature data on rostral auditory centers in amniotes with a focus on their core–belt neural organization, as related to lemniscal (core) and extralemniscal or non-lemniscal (belt) pathways. Our immunohistochemical results on the distribution of the calcium-binding proteins, parvalbumin (PV) and calbindin (CB), in the pigeon mesencephalic (MLD) and thalamic (Ov) auditory centers clearly demonstrate the presence of this cytoarchitectonic pattern of neural organization in birds. We analyze its functional significance for the optimal integration of the results of perceptual auditory information processing and its affective assessment due to neural connections between the belt regions of auditory centers and limbic centers. In the latter, specifically in the amygdala, there are audiomotor and audiovegetative relays responsible for the choice and implementation of behavioral types most adequate to each given context. A comparative analysis of different characteristics of auditory centers across a broad range of vertebrates allows hypothesizing about the origin, conservation and transformation of the core and belt regions of auditory centers during evolution.

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Abbreviations

СаВРr:

calcium-binding proteins

СВ:

calbindin

DVR:

dorsal ventricular ridge

C:

inferior colliculus

ICC:

nucleus centralis of the IC

ICS:

nucleus superficialis of the IC

ICX:

nucleus externus of the IC

ir:

immunoreactive

L:

telencephalic auditory nucleus-field

L2:

central lamina of the L

L1, L3:

peripheral laminae of the L

MGB:

corpus geniculatum mediale

MLD:

nucleus mesencephalicus lateralis, pars dorsalis

Mp:

nucleus medialis posterior

nCe:

nucleus centralis Ov

Ov:

nucleus ovoidalis

Ovl:

nucleus ovoidalis, pars lateralis

Ovm:

nucleus ovoidalis, pars medialis

PV:

parvalbumin

Re:

nucleus reuniens

tOv:

tractus ovoidalis

REFERENCES

  1. Hu, B., Functional organization of lemniscal and non-lemniscal auditory thalamus, Exp. Brain Res., 2003, vol. 193, pp. 543–549. https://doi/org/10.1007/s00221-003-1611-5

  2. Lee, C.C., Exploring functions for the non-lemniscal auditory thalamus, Front. Neural. Circuits, 2015, vol. 9, p. 69. https://doi.org/10.3389/fncir.2015.00069.

  3. Ito, T. and Malmierca, M.S., Neurons, connections and microcircuits of the inferior colliculus, The Mammalian Auditory Pathways, Springer Verlag, New York, 2018, pp. 127–157. https://doi.org/10.1007/978-1-4612-4416-5

  4. Aitkin, L.M., Webster, W.R., Veale, J.L., and Crosby, D.C., Inferior colliculus. I. Comparison of response properties in central, pericentral and external nuclei of adult cat, J. Neurophysiol., 1975, vol. 38, pp. 1196–1207. https://doi.org/10.1152/jn.1975.38.5.1196

  5. Сassaday, J.H., Diamond, I.T., and Harting, J.K., Auditory pathway to the cortex in Tupaia glis, J. Comp. Neurol., 1976, vol. 166(3), pp. 303–340. https://doi.org/10.1002/cne.901660304

  6. Kudo, M. and Niimi, K., Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques, Brain Res., 1978, vol. 155(1), pp. 113–117. https://doi.org/10.1016/0006-8993(78)90310-4

  7. Anderson, R.A., Roth, G.L., Aitkin, L.M., and Merzeniel, M.M., The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat, J. Comp. Neurol., 1980, vol. 194(3), pp. 649–662. https://doi.org/10.1002/cne.901940311

  8. Aitkin, L.M., Kenyon, C.E., and Philpott, P., The representation of the auditory and somatosensory systems in the external nucleus in the cat colliculus inferior, J. Comp. Neurol., 1981, vol. 196, pp. 25–40. https://doi.org/10.1002/cne.901960104

  9. Califord, M.B. and Aitkin, L.M., Ascending projections to the medial geniculate body of the cat: evidence for multiple auditory pathways through thalamus, J. Neurosci., 1983, vol. 3(11), pp. 2865–2880. https://doi.org/10.1523/JNEUROSCI.03-11-02365.1983

  10. Tokunaga, A., Sugita, S., and Otani, K., Auditory and nonauditory subcortical afferents to the inferior colliculus in the rat, J. Hirnforsch., 1984, vol. 25, pp. 461–472. PMID: 6481158

  11. Gruters, K.G. and Groh, J.M., Sounds and beyond: multisensory and other non-auditory signals in the inferior colliculus, Front. Neural Circuits, 2012, vol. 6, p. 96. PMID: 23248584 PMCID: PMC3518932. https://doi.org/10.3389/fncir.2012.00096

  12. Bartlett, E.L., The organization and physiology of the auditory thalamus and its role in the processing acoustic features for speech reception and language, Brain and Language, 2013, vol. 126, pp. 29–48. https://doi.org/10.1016/j.bandl.2013.03.003

  13. Jones, E.G., Viewpoint: the core and matrix of thalamic organization, Neurosci., 1998, vol. 85(2), pp. 331–345. https://doi.org/10.1016/S0306-4522(97)00581-2

  14. Grothe, B., Carr, C.E., Cassaday, J.H., Fritsch, B., and Köppl, C., The evolution of central pathways and their neural processing patterns, Evolution of Vertebrate Auditory System, Springer Verlag, New York, 2004, pp. 289–359. https://doi.org/10.1007/978-1-4419-8957-4

  15. Zeng, S.-J., Lin, Y.-T., Tian, C.-P., Song, K.-J., Zhang, X.-W., and Zuo, M.-X., Evolutionary significance of delayed neurogenesis in the core versus shell auditory areas of Mus musculus, J. Comp. Neurol., 2009, vol. 515(5), pp. 600–613. https://doi.org/10.1002/cne.22076.

  16. Nakamura, S., Marumi, T., Tsutsui, K., and Lijima, T., Difference in the functional significance between the lemniscal and paralemniscal pathways in the perception of direction of single-wisker stimulation examined by muscimol microinjection, Neurosci. Res., 2009, vol. 64(3), pp. 323–329. https://doi.org/10.1016/j.neures.2009.04.005

  17. Lee, C.C. and Sherman, S.M., On the classification of the pathways in the auditory midbrain, thalamus and cortex, Hear. Res., 2011, vol. 276(1–2), pp. 79–87. https://doi.org/10.1016/j.heares.2010.12.012

  18. Straka, M.M., Schmitz, S., and Lim, H.H., Response features across the auditory midbrain reveal an organization consistent with a dual lemniscal pathway, J. Neurophysiol., 2014, vol. 112(4), pp. 981–988. https://doi.org/10.1152/jn.00008.2014

  19. Oliver, D.L. and Hall, W.C., The medial geniculate body of the tree shrew, Tupaia glis, II. Connections with the neocortex, J. Comp. Neurol., 1978, vol. 182, pp. 4459–4493. https://doi.org/10.1002/cne.901820306

  20. Coleman, J.R. and Clerici, W.J., Sources of projections to subdivisions of the inferior colliculus in the rat, J. Comp. Neurol., 1987, vol. 262(2), pp. 215–226. https://doi.org/10.1002/cne.902620204

  21. Le Doux, J.E., Ruggiero, D.A., and Reis, D.J., Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat, J. Comp. Neurol., 1987, vol. 264(1), pp. 123–146. https://doi:10.1002/cne.902640110

  22. Le Doux, J.E., Farb, C., and Ruggiero, D.A., Topographic organization of. neurons in the acoustic thalamus that project to the amygdale, J. Neurosci., 1990, vol. 10(4), pp. 1043–1054. https://doi.org/10.1523/JNEUROSCI.10-04-01043.1990

  23. Shinonaga, Y., Takada, M., and Mizuno, N., Direct projections from non-laminated divisions of medial geniculate nucleus to the temporal polar cortex and amygdale in the cat, J. Comp. Neurol., 1994, vol. 340(3), pp. 405–426. https://doi.org/10.1002/cne.903400310

  24. Campeau, S. and Davis, M., Involvment of subcortical and cortical afferents to the lateral nucleus of the amygdale in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli, J. Neurosci., 1995, vol. 15(3), pp. 2312–2327. https://doi.org/10.1523/JNEUROSCI.15-03-02312.1995

  25. Linke, R., Braune, G., and Schwegler, H., Differential projection of posterior paralaminar thalamic nuclei to the amygdaloid complex in the rat, Exp. Brain Res., 2000, vol. 138(1), pp. 135–138. https://doi.org/10.1007/s002210000475

  26. Jones, E.G., Chemically defined parallel pathways in the monkey auditory system, Ann. N.Y. Acad. Sci., 2003, vol. 999, pp. 218–233. https://doi.org/10.1196/annals.1284.033

  27. Zhou, J. and Shore, S., Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig, J. Comp. Neurol., 2006, vol. 495(1), pp. 100–112. https://doi.org/10.1002/cne.20863

  28. Anderson, L.A., Wallace, N.M., and Palmer, A.R., Identification of subdivisions in the medial geniculate body of the guinea pig, Hear. Res., 2007, vol. 228(1–2), pp. 156–167. https://doi.org/10.1016/j.heares.2007.02.005

  29. Künzle, H., Amygdaloid connections in the lesser hedgehog tenrec, Brain Struct. Funct., 2012, vol. 217(1), pp. 141–164. https://doi.org/10.1007/s00429-011-0328-7

  30. Tsvetkov, E.A., Vesselkin, N.P., Krasnoshchekova, E.I., and Kharazova, A.D., Amigdala: neuroanatomy and neurophysiology of fear, J. Evol. Biochem. Physiol., 2015, vol. 51(6), pp. 456–470. https://doi.org/10.1134/S0022093015060022

  31. Pandya, D.N., Anatomy of the auditory cortex, Rev. Neurol., 1995, vol. 151(8–9), pp. 486–494. PMID: 8578069

  32. Cruikshank, S.J., Killackey, H.P., and Metherate, R., Parvalbumin and calbindin are differently distributed within primary and secondary subdivisions of the mouse auditory forebrain, Neurosci., 2000, vol. 105(3), pp. 553–569. https://doi.org/10.1016/S0306-4522(01)00226-3

  33. Budinger, E., Hell, P., and Scheich, H., Functional organization of the auditory cortex of Mongolian gerbil (Meriones unguclatus), IV. Connections with anatomically characterized subcortical structures, Eur. J. Neurosci., 2001, vol. 12(5), pp. 2452–2474. https://doi.org/10.1046/j.1460-9568.2000.00143.x

  34. Pienkowski, M. and Harrison, R.V., Tone response in core versus belt auditory cortex in developing chinchilla, J. Comp. Neurol., 2005, vol. 492(1), pp. 101–199. https://doi.org/10.1002/cne.20708

  35. De la Mothe, L.A., Blumell, S., Kajikawa, Y., and Hackett, TA., Thalamic connections of auditory cortex in marmoset monkeys: lateral belt and parabelt regions, Anat. Rec., 2012, vol. 295(5), pp. 822–836. https://doi.org/10.1002/ar.22454

  36. Smith, P.H., Ulrich, D.J., Manning, K.A., and Banks, M.I., Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate body, J. Comp. Neurol., 2012, vol. 520(1), pp. 34–51. https://doi.org/10.1002/cne.22682

  37. Kaas, J.H., The evolution of brains from early mammals to human, Wires Cog. Sci., 2013, vol. 4, pp. 33–45. https://doi.org/10.1002/wcs.1206

  38. Cuello, A.C. and Kanazawa, I., The distribution of substance P immunoreactive fibers in the rat central nervous system, J. Comp. Neurol., 1978, vol. 178(1), pp. 129–156. https://doi.org/10.1002/cne.901780108

  39. Durand, S.E., Zuo, M.X., Zhou, S.L., and Cheng, M.-F., Avian auditory pathways show met-enkephalin-like immunoreactivity, Neuroreport, 1993, vol. 4(6), pp. 727–730. https://doi.org/10.1097/00001756-199306000-00032

  40. Zeng, S.-J., Li, J., Zhang, X., and Zuo, M., Distinction of neurochemistry between the cores and their shells of auditory nuclei in tetrapode species, Brain Behav. Evol., 2007, vol. 70(1), pp. 1–20. https://doi.org/10.1159/000101066

  41. Sharma, V., Nag, T.C., Wadhwa, S., and Roy, T.S., Stereological investigation and expression of calcium binding proteins in developing human inferior colliculus, J. Chem. Neuroanat., 2009, vol. 37(2), pp. 78–86. https://doi.org/10.1016/j.jchemneu.2008.11.002

  42. Cai, D., Yue, Y., Su, X., Liu, M., Wang, Y., You, L., Xie, F., et al., Distinct anatomical connectivity patterns differentiate subdivisions of nonlemniscal auditory thalamus in mice, Cerebral Cortex, 2019, vol. 29(6), pp. 2437–2454. https://doi.org/10.1093/cercor/bhy115

  43. Gonzalez-Lima, F. and Cada, A., Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study, Neurosci., 1994, vol. 63(2), pp. 559–578. https://doi.org/10.1016/0306-4522(94)90550-9

  44. Okoyama, S., Oubayashi, M., Ito, M., and Harad, S., Neuronal organization of the rat inferior colliculus participating in four auditory pathways, Hear. Res., 2006, vol. 218(1–2), pp. 72–80. https://doi.org/10.1016/j.heares.2006.04.004

  45. Anderson, A., Wallace, N.M., and Palmer, A.R., Identification of subdivisions in the medial geniculate body of the guinea pig, Hear. Res., 2007, vol. 228(1–2), pp. 156–167. https://doi.org/10.1016/j.heares.2007.02.005

  46. Carr, С.E. and Soares, D.D., Shared features of the auditory system of birds and mammals, Evolution of the Nervous System, Non-Mammalian Vertebrates, vol. 1, Acad. Press Elsevier, Amsterdam, 2017, pp. 443–457.

  47. Knudsen, E.I., Subdivisions of the inferior colliculus in the barn owl (Tyto alba), J. Comp. Neurol., 1983, vol. 218(2), pp. 174–186. https://doi.org/10.1002/cne.902180205

  48. Wagner, H., Güntürkün, O., and Nieder, B., Anatomical markers for the subdivisions of the barn owl’s inferior colliculus complex and adjacent peri- and subventricular structures, J. Comp. Neurol., 2003, vol. 465(1), pp. 145–159. https://doi.org/10.1002/cne.10826

  49. Logerot, P., Krützfeldt, N.O.E., Wild, J.M., and Kubke, M.F., Subdivisions of the auditory midbrain (n. mesencephalicus lateralis, pars dorsalis) in zebra finches using calcium-binding protein immunocytochemistry, PloS One, 2011, vol. 6, e 20686. https://doi.org/10.1371/journal.pone.0020686

  50. Niederleitner, B. and Luksch, H.J., Neuronal morphology in subdivisions of the inferior colliculus of chicken (Gallus gallus), J. Chem. Neuroanat., 2012, vol. 44(1), pp. 24–33. https://doi.org/10.1016/j.jchemneu.2012.03.004

  51. Braun, K., Scheich, H., Schachner, M., and Heizmann, C.W., Distribution of parvalbumin, cytochrome oxidase activity and 14 C-2-desoxyglucose uptake of the zebra finch. I. Auditory and vocal motor systems, Cell Tissue Res., 1985, vol. 240, pp. 101–115. https://doi.org/10.1007/BF00217563

  52. Dezso, A., Schwarz, D.W., and Schwarz, I.E., A survey of the auditory midbrain, thalamus and forebrain in the chicken (Gallus domesticus) with cytochrome oxidase histochemistry, J. Otolaryngol., 1993, vol. 22(5), pp. 391–396. PMID: 8283511

  53. Puelles, L., Robles, C., Martinez-de-la-Torre, M., and Martinez, S., New subdivisions scheme for avian torus semicircularis: histochemical maps in the chick, J. Comp. Neurol., 1994, vol. 340(1), pp. 98–125. https://doi.org/10.1002/cne.903400108

  54. Wild, J.M., Convergence of somatosensory and auditory projections in the avian torus semicircularis, including the central auditory nucleus, J. Comp. Neurol., 1995, vol. 358(4), pp. 465–486. https://doi.org/10.1002/cne.903580402

  55. Lanuza, E., Davies, D.C., Landete, J.M., Novejarque, A., and Martinez-Garcia, F., Distribution of CGRP-like immunoreactivity in the chick and quail brain. J. Comp. Neurol., 2000, vol. 421 (4), pp. 515–532. https://www.researchgate.net/deref/http%3A%2F%2Fdx.doi.org%2F10.1002%2F(SICI)1096-9861(20000612)421%3A4%3C515%3A%3AAID-CNE4%3E3.0.CO%3B2-6

  56. Zeng, S.J., Lin, Y.T., Yang, L., Zhang, X.W., and Zuo, M.X., Comparative analysis of neuronogenesis between core and shell regions in the chick (Gallus gallus domesticus), Brain Res., 2008, vol. 1216, pp. 24–37. https://doi.org/10.1016/j.brainres.2008.04.012

  57. Lovell, P.V. and Mello, C.V., Brain expression of cholecystokinin in the zebra finch (Taenioppigia guttata), J. Comp. Neurol., 2011, vol. 519(2), pp. 211–237. https://doi.org/10.1002/cne.22513

  58. Belekhova, M.G., Kenigfest, N.B., Chudinova, T.V., and Vesselkin, N.P., Distribution of calcium-binding proteins, parvalbumin and calbindin, in the midbrain auditory centre (MLd) of a pigeon, Dokl. Biol. Sci., 2016, vol. 466, pp. 1–4. https://doi.org/10.1134/S001249661601004

  59. Brauth, S.E., Investigation of central auditory nuclei in the budgerigar with cytochrome oxidase histochemistry, Brain Res., 1990, vol. 508(1), pp. 142–146. https://doi.org/10.1016/0006-8993(90)91127-3

  60. Durand, S.E., Tepper, J.M., and Cheng, M.F., The shell region of the nucleus ovoidalis: a subdivision of avian auditory thalamus, J. Comp. Neurol., 1992, vol. 323(4), pp. 495-518. https://doi.org/10.1002/cne.903230404

  61. Wild, J.M., Karten, H.J., and Frost, B.J., Connections of the auditory forebrain in the pigeon (Columba livia), J. Comp. Neurol., 1993, vol. 337(1), pp. 32–62. https://doi.org/10.1002/cne.903370103

  62. Cheng, M.F. and Zuo, M.X., Proposed pathway for vocal self-stimulation: met-enkephalinergic projections linking the midbrain vocal nucleus, auditory responsive thalamic regions and neurosecretory hypothalamus, J. Neurobiol., 1994, vol. 25(4), pp. 361–379. https://doi.org/10.1002/neu.480250403

  63. Proctor, L. and Konishi, M., Representation of sound localization cues in the auditory thalamus of the barn owl, Proc. Nat. Acad. Sci. USA, 1997, vol. 94(19), pp. 1021–1025. https://doi.org/10.1073/pnas.94.19.10421

  64. Cheng, M.F. and Peng, J.P., Reciprocal call between the auditory thalamus and the hypothalamus: an antidromic study, Neuroreport, 1997, vol. 8(3), pp 653–658. https://doi.org/10.1097/00001756-199702100-00015

  65. Zeng, S., Zhang, X., Peng, W., and Zuo, M.X., Immunohistochemistry and neural connectivity of the Ov shell in song-bird and their evolutionary implications, J. Comp. Neurol., 2004, vol. 470(2), pp. 192–209. https://doi.org/10.1002/cne.11042

  66. Brauth, S.E., Liang, W., and Hall, W.S., Contact-call driven and tone-driven zenk expression in the nucleus ovoidalis of the budgerigar (Melopsittacus undulatus), Neuroreport, 2006, vol. 17(13), pp. 1407–1410. https://psycnet.apa.org/doi/10.1097/01.wnr.0000233105.28279.fa

  67. Belekhova, M.G., Chudinova, T.V., and Kenigfest, N.B., Metabolic activity of pigeon thalamic auditory centers, J. Evol. Biochem. Physiol., 2009, vol. 45(5), pp. 619–626. https://doi.org/10.1134/S0022093009050090

  68. Belekhova, M.G., Chudinova, T.V., and Kenigfest, N.B., Distribution of calcium-binding proteins parvalbumin and calbindin in the thalamic auditory center in pigeons, J. Evol. Biochem. Physiol., 2016, vol. 52(6), pp. 482–489. https://doi.org/10.1134/S1234567816060070

  69. Wang, Y., Zorio, D.F.R., and Karten, H.J., .Heterogeneous organization and connectivity of the chicken auditory thalamus (Gallus gallus), J. Comp. Neurol., 2017, vol. 525(14), pp. 3044–3071. https://doi.org/10.1002/cne.24262

  70. Cheng, M.F., Chalken, M., Zuo, M., and Miller, H., Nucleus taeniae of amygdale of birds; an anatomical and functional studies in ring dove (Streptopelia risoria) and European starling (Sturnus vulgaris), Brain Behav. Evol., 1999, vol. 53 (5–6), pp. 249–270. https://doi.org/10.1159/000006597

  71. Cheng, M.F. and Durand, S.E., Song and limbic brain: a new function for the birds own song, Ann. NY Acad. Sci., 2004, vol. 1016, pp. 611–627. https://doi.org/10.1196/annals.1298.019

  72. Ikebushi, I., Hasegawa, T., and Bischof, H.J., Amygdala and socio-sexual behavior in male zebra finches, Brain Behav. Evol., 2009, vol. 74(4), pp. 250–257. https://doi.org/10.1159/000264660

  73. Atoji, Y. and Wild, J.M., Afferent and efferent projections of the central caudal nidopallium in the pigeon, J. Comp. Neurol., 2009, vol. 517, pp. 350–370. https://doi.org/10.1159/000264660

  74. Atoji, Y. and Wild, J.M., Afferent and efferent projections of the mesopallium in the pigeon (Columba livia), J. Comp. Neurol., 2012, vol. 520(4), pp. 717–741. https://doi.org/10.1002/cne.22763

  75. Fuji, T.G., Ikebushi, I., and Okanoya, K., Auditory responses to vocal sounds in the song bird nucleus taeniae of the amygdala and adjacent arcopallium, Brain Behav. Evol., 2016, vol. 87(4), pp. 275–289. https://doi.org/10.1159/000447233

  76. Zettel, M.L., Frizina, R.D., Haider, S.E., and O’Neill, W.E., Age-related changes in calbindin and calretinin immunoreactivity in the inferior colliculus of CBA/Ca J and C57B 1/6 mice, J. Comp. Neurol., 1997, vol. 386(1), pp. 92–110. https://doi.org/10.1002/(SICI)1096-9861(19970915)386:1%3C92::AID-CNE9%3E3.0.CO;2-8

  77. Kelley, P.E., Frizina, R.D., Zettell, M.L., and Walton, J.P., Differential calbindin-like immunoreactivity in the brainstem auditory of the chinchilla, J. Comp. Neurol., 1992, vol. 320(2), pp. 196–212. https://doi.org/10.1002/cne.903200205

  78. Vater, M. and Braun, K., Parvalbumin, calbindin D-28k and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats, J. Comp. Neurol., 1994, vol. 341(4), pp. 534–558. https://doi.org/10.1002/cne.903410409

  79. De Venecia, R.K., Smelser, C.B., and McMullen, N.T., Parvalbumin is expressed in a reciprocal circuit linking the medial geniculate body and auditory neocortex in the rabbit, J. Comp. Neurol., 1998, vol. 400(3), pp. 349–362. https://doi.org/10.1002/(sici)1096-9861(19981026)400:3%3C349::aid-cne5%3E3.3.co;2-c

  80. Tardif, E., Chiry, O., Probst, A., Magistretti, P.J., and Clarke, S., Patterns of calcium-binding proteins in human inferior colliculus: identification of subdivisions and evidence for putative parallel systems, Neurosci., 2003, vol. 116(4), pp. 1111–1121. https://doi.org/10.1016/S0306-4522(02)00774-1

  81. del Campo, H.M., Measor, K., and Razak, K.A., Parvalbumin and calbindin expression in parallel thalamocortical pathways in a gleaning bat, Antrozous pallidus, J. Comp. Neurol., 2014, vol. 522(10), pp. 2431–45. https://doi.org/10.1002/cne.23541.

  82. Campos, L.M.G., Osorio, E.C., da Silva Santos, G.L., Nogueira, M.J., et al., Temporal changes in calcium binding proteins in the medial geniculatus nucleus of the monkey Sepajus paella, J. Chem. Neuroanat., 2015, vol. 68, pp. 45–54. https://doi.org/10.1016/j.jchemneu.2015.07.005

  83. Takahashi, T.T., Carr, C.E., Brecha, N., and Konishi, M., Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl, J. Neurosci., 1987, vol. 7(6), pp. 1843–1856. https://doi.org/10.1523/JNEUROSCI.07-06-01843.1987

  84. Heizmann, C.W. and Braun, K., Calcium binding proteins. Molecular and functional aspects. The Role of Calcium in Biological Systems, CRC Press Inc., Roca Raton, FL, 1990, pp. 21–65.

  85. Braun, K., Scheich, H., Heizmann, C.W., and Hunziker, W., Parvalbumin and calbindin-D-28k immunoreactivity as developmental markers of auditory and vocal motot nuclei of the zebra finch, Neurosci., 1991, vol. 40(3), pp. 853–869. https://doi.org/10.1016/0306-4522(91)90017-I

  86. Pinaud, R., Saldanha, C.J., Wynne, R.D., Lovell, P.V., and Mello, C.V., The excitatory thalamo-“cortical” projection within the song control system of zebra finches is formed by calbindin-expressing neurons, J. Comp. Neurol., 2007, vol. 504(6), pp. 601–618. https://doi.org/10.1002/cne.21457

  87. Cant, N.B. and Benson, C.G., Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculats, J. Comp. Neurol., 2007, vol. 503(3), pp. 432–453. https://doi.org/10.1002/cne.21391

  88. Wang, Y. and Karten, H.J., Three subdivisions of the auditory midbrain in chicks (Gallus gallus) identified by their afferent and commissural projections, J. Comp. Neurol., 2010, vol. 518(8), pp. 1199–1219. https://doi.org/10.1002/cne.22269

  89. Storace, D.A., Higgins, N.C., and Read, H.L., Thalamic label patterns suggest primary band ventral auditory fields are distinct core regions, J. Comp. Neurol., 2010, vol. 518(10), pp. 1630–1647. https://doi.org/10.1002/cne.22345

  90. Guillery, R.W. and Sherman, S.M., The thalamus as a motor output, Phil. Trans. R Soc. Lond., 2002, vol. 357(1428), pp. 1809–1821. https://dx.doi.org/10.1098%2Frstb.2002.1171

  91. Guillery, R.W., Anatomical pathways that link perception and action, Progr. Brain Res., 2005, vol. 149, pp. 235–256. https://doi.org/10.1016/s0079-6123(05)49017-2

  92. Medina, L., Abellan, A., and Desfilis, E., Evolution of pallial areas and networks involved in sociality: comparison between mammals and sauropsids, Front. Physiol., 2019, vol. 10, p. 894. https://doi.org/10.3389/fphys.2019.00894

  93. Doron, N.N. and Le Doux, J.E., Organization of projections to the lateral amygdale from auditory and visual areas of the thalamus in the rat, J. Comp. Neurol., 1999, vol. 412(3), pp. 383–409. PMID: 10441229

  94. Le Doux, J.E., Emotion circuits in the brain, Ann. Rev. Neurosci., 2000, vol. 23, pp. 155–184. https://doi.org/10.1146/annurev.neuro.23.1.155

  95. Pesoa, L., Emotion and cognition and the amygdale: from “what is it? To ”what to be done?”, Neuropsychol., 2010, vol. 48(12), pp. 3416–3429. https://dx.doi.org/10.1016%2Fj.neuropsychologia.2010.06.038

  96. Gadziolla, M.A., Shandhag, S.I., and Wenstrup, J.J., Two distinct representations of social vocalization in the basolateral amygdale, J. Neurophysiol., 2016, vol. 115(2), pp. 868–886. https://dx.doi.org/10.1152%2Fjn.00953.2015

  97. Mukhina, Ju.K., Afferent connections of the basolateral region of the cat brain amygdaloid complex, Arkh. Anat. Gistol. Embriol., 1985, vol. 88, pp. 25–34.

  98. Mascagni, F., McDonald, A.J., and Coleman, J.R., Corticoamygdaloid and corticocortical projections of the rat temporal cortex: a Phaseolus vulgaris leucoagglutinin study, Neurosci., 1993, vol. 57(3), pp. 697–715. https://doi.org/10.1016/0306-4522(93)90016-9

  99. Li, X.F., Stutzmann, G.F., and Le Doux, J.E., Convergent but temporally separated inputs to lateral amygdale from the auditory thalamus, Learn. Mem., 1996, vol. 3(2–3), pp. 229–242. https://doi.org/10.1101/lm.3.2-3.229

  100. Antunes, R. and Moita, M.A., Discriminative auditory fear learning recuires both tuned and nontuned auditory pathways to the amygdale, J. Neurosci., 2010, vol. 30(29), pp. 9782–9787. https://doi.org/10.1523/jneurosci.1037-10.2010

  101. Janak, P.H. and Tue, K.M., From circuits to behavior in amygdale, Nature, 2015, vol. 517(7534), pp. 284–292. https://doi.org/10.1038/nature14188

  102. Bergstrom, H.C. and Johnson, L.R., An organization of visual and auditory fear conditioning in the lateral amygdale, Neurobiol. Learn. Memory, 2014, vol. 116, pp. 1–13. https://doi.org/10.1016/j.nlm.2014.07.008

  103. Saddors, M.P., Gallagher, M., and Schoenbaum, G., Rapid associative encoding in basolateral amygdale depends on connections with orbitofrontal cortex, Neuron, 2005, vol. 46(2), pp. 321–331. https://doi.org/10.1016/j.neuron.2005.02.018

  104. Rudebeck, P.H., Walton, M.E., Millette, B.H., Shirley, E., Rushwworth, M.F., and Bannerman, D.H., Distinct contribution of frontal areas to emotional and social behavior in the rat, Eur. J. Neurosci., 2007, vol. 26(8), pp. 2315–2326. https://doi.org/10.1111/j.1460-9568.2007.05844.x

  105. Lichtenberg, N.T., Pennigton, Z.T., Holley, S.M., Greenfield, V.Y., Cepeda, C., et al., Basolateral amygdala to orbitofrontal projections enable cue-triggered reward expectations, J. Neurophysiol., 2017, vol. 37(35), pp. 8374–8384. https://doi.org/10.1523/jneurosci.0486-17.2017

  106. Sander, K., Bechmann, A., and Scheich, H., Audition of laughing and crying leads to right amygdale activation in a low noise fMRI setting, Brain Res. Brain Res. Prot., 2003, vol. 11(2), pp. 81–91. https://doi.org/10.1016/s1385-299x(03)00018-7

  107. Naumann, R.T. and Kanwal, J.S., Basolateral amygdala respond robustly to social calls: spiking characteristics of single unit activity, J. Neurophysiol., 2011, vol. 105(2), pp. 2389–2404. https://doi.org/10.1152/jn.00580.2010

  108. Fruhholz, S., Trost, W., and Grandjean, D., The role of medial temporal limbic system in voice and music, Progr. Neurobiol., 2014, vol. 123, pp. 1–17. https://doi.org/10.1016/j.pneurobio.2014.09.003

  109. Zhao, Y., Sun, Q., Chen, G., and Yang, J., Hearing emotional sounds: category representation in the human amygdale, Soc. Neurosci., 2018, vol. 13(1), pp. 117–128. https://doi.org/10.1080/17470919.2016.1267040

  110. Xiao, C., Liu, Y., Xu, J., Can, X., and Xiao, Z., Septal and hippocampal neurons contribute to auditory relay and fear conditioning, Front. Cell. Neurosci., 2018, vol. 12, 102(1–17). https://doi.org/10.3389/fncel.2018.00102

  111. Reiner, A., Perkel, D.J., Bruce, L.L., Butler, A.B., Csillag, A., et al., Avian brain nomenclature forum, Revised nomenclature for avian telencephalon and some other related brainstem nuclei, J. Comp. Neurol., 2004, vol. 473(3), pp. 377–414. https://doi.org/10.1002/cne.20118

  112. Martinez-Garcia, F., Novejarque, A., and Lanuza, E., Evolution of the amygdala in vertebrates, Evolution of the Nervous System, vol. 2, Nonmammalian vertebrates, Academic Press Elsevier, Amsterdam, 2007, pp. 255–334.

  113. Saint-Dizier, H., Constantin, P., Davies, D.C., Leterrier, C., Lévy, F., and Richar, S., Subdivisions of the arcopallium posterior amygdale complex are differentially involved in the control of fear behavior of the Japanese quail, Brain Res. Bull., 2009, vol. 79(5), pp. 288–295. https://doi.org/10.1016/j.brainresbull.2009.03.004

  114. Xin, Q., Ogura, Y., and Uno, L., and Matsushima, T., Selective contribution of the telencephalic arcopallium to the social facilitation of foraging efforts in the domestic chick, Eur. J. Neurosci., 2017, vol. 45(3), pp. 365–380. https://doi.org/10.1111/ejn.13475

  115. Daffers, R., Active avoidance behavior following archistriatal lesions in pigeon, J. Comp. Physiol. Psychol., 1975, vol. 89(10), pp. 1169–1179. https://doi.org/10.1037/h0077181

  116. Lowndes, M. and Davis, D.C., The effect of archistriatal lesion on one trial passive avoidance learning in chick, Eur. J. Neurosci., 1994, vol. 6(4), pp. 525–530. https://doi.org/10.1111/j.1460-9568.1994.tb00296.x

  117. Lowndes, M. and Davis, D.C., The effect of archistriatal lesion on “open-field” and fear/avoidance behavior in the domestic chick, Behav. Brain Res., 1995, vol. 72(1–2), pp. 25–32. https://doi.org/10.1016/0166-4328(95)00026-7

  118. Gao, M., Lengersdorf, D., Stüttgen, M.C., and Güntürkün, O., NMDA receptors in the avian amygdale and premotor arcopallium mediate distinct aspects of appetitive learning, Behav. Brain Res., 2018, vol. 343, pp. 71–82. https://doi.org/10.1016/j.bbr.2018.01.026

  119. Vates, G.E., Broome, B.M., Mello, C.V., and Nottebohm, F., Auditory pathways of caudal telencephalon and their relation to the song system of adult male finches (Taeniopygia guttata), J. Comp. Neurol., 1996, vol. 366(4), pp. 613–642. https://doi.org/10.1002/(sici)1096-9861(19960318)366:4%3C613::aid-cne5%3E3.0.co;2-7

  120. Genter, T.Q., Hulse, S.H., and Ball, G.F., Functional differences in forebrain auditory regions during learned vocal recognition in songbirds, J. Comp. Physiol. A, 2004, vol. 190(12), pp. 1001–1010. https://doi.org/10.1007/s00359-004-0556-x

  121. Sadananda, M., Korte, S., and Bischof, H.J., Afferentation of a caudal forebrain area activated during courtship behavior: a tracing study in the zebra finch (Taeniopygia guttata), Brain Res., 2007, vol. 1184, pp. 108–120. https://doi.org/10.1016/j.brainres.2007.09.040

  122. Prather, J.F., Auditory signal processing in communication: perception and performance of vocal sounds, Hear. Res., 2013, vol. 305, pp. 144–155. https://doi.org/10.1016/j.heares.2013.06.007

  123. Calabrese, A. and Woolsey, S.M.N., Coding principles of the canonical cortical microcircuit in the avian brain, Proc. Natl. Acad. Sci. USA, 2015, vol. 112(11), pp. 3517–3522. https://doi.org/10.1073/pnas.1408545112

  124. Danning, J.l., Maze, S.E., Atwood, E.J., and Prather, J.F., Caudal mesopallial neurons in female songbirds bridge sensory and motor brain regions, J. Comp. Neurol., 2018, vol. 526(10), pp. 1703–1711. https://doi.org/10.1002/cne.24440

  125. Pritz, M.B., Ascending connections of a midbrain auditory area in a crocodile, Caiman crocodilius, J. Comp. Neurol., 1974, vol. 153(2), pp. 179–193. https://doi.org/10.1002/cne.901530204

  126. Foster, R.E. and Hall, W.C., The organization of auditory pathways in a reptile Iguana iguana, J. Comp. Neurol., 1978, vol. 178(4): 783–832. https://doi.org/10.1002/cne.901780412

  127. Browner, R.H., Kennedy, M.C., and Facelle, T., The cytoarchitecture of the torus in the red-eared turtle, J. Comp. Neurol., 1981, vol. 169(2), pp. 207–223. https://doi.org/10.1002/jmor.1051690207

  128. Butler, A.B. and Bruce, L.L., Nucles laminaris of the torus semicircularis: projection to the spinal cord in reptiles. Neurosci. Lett., 1981, 25(3), pp. 221–226. https://doi.org/10.1016/0304-3940(81)90395-5

  129. Woodson, W. and Künzle, H., Distribution and structural characterization of neurons giving rise to descending spinal projections in the turtle, Pseudemys scripta elegans, J. Comp. Neurol., 1982, vol. 212(4), pp. 336–348. https://doi.org/10.1002/cne.902120403

  130. Belekhova, M.G., Zharskaya, V.D., Khachunts, A.S., Gaidaenko, G.V., and Tumanova, N.L., Connectionss of the mesencephalic, thalamic and telencephalic auditory centers in turtles: Some structural bases for audisomatic interrelations, J. Hirnforsch. B, 1985, vol. 26(2), pp. 127–152. PMID: 2410486

  131. Künzle, H., Projections from the cochlear nuclear complex to rhombencephalic auditory centers and inferior colliculus in the turtle, Brain Res., 1986, vol. 379, pp. 307–319. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0020686#

  132. Pritz, M.B. and Stritzel, M.E., A second auditory area in the non-cortical telencephalon of a reptile, Brain Res., 1992, vol. 569(1), pp. 146–151. https://doi.org/10.1016/0006-8993(92)90381-i

  133. Belekhova, M.G., Thalamo-amygdaloid auditory–somatosensory projections are primitive conservative brain character of amniotes (an analysis of literature and own data, a hypothesis), Zh. Evol. Biokhim. Fiziol., 1994, vol. 30, pp. 454–473.

  134. Diaz, C., Yanes, C., Trujillo, C.M., and Puelles, L., Cytoarchitectonic subdivisions in the subtectal midbrain of the lizard Gallotia Galotti, J. Neurocytol., 2000, vol. 29(8), pp. 569–593. https://doi.org/10.1023/a:1011067918585

  135. Khachunts, A.S., Electrophysiological characteristics of representation of auditory and somatosensory systems in the turtle midbrain, Neurophysiol., 1983, vol. 14, pp. 191–198. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0020686#

  136. Khachunts, A.S. and Belekhova, M.G., Characteristics of representations of the auditory and somatosensory systems in the thalamus of the turtle: an electrophysiological study, Neurophysiol., 1986, vol. 18(4), pp. 443–453. PMID: 3762789

  137. Belekhova, M.G., Chudinova, T.V., Repérant, J., Ward, R., Jay, B., Vesselkin, N.P., and Kenigfest, N.B., Core-and-belt organization of the mesencephalic and forebrain auditory centres in turtles: expression of calcium-binding proteins and metabolic activity, Brain Res., 2010, vol. 1345, pp. 84–102. https://doi.org/10.1016/j.brainres.2010.05.026

  138. Xi, C., Chen, Q., Zeng, S.-J., Lin, Y.-T., Huang, Y.-F., Kiu, Y., Zhang, X.-W., and Zuo, M.X., Sites of origin and developmental core and shell regions of torus semicircularis in the Chinese softshell turtle (Pelodiccus sinensis), J. Comp. Neurol., 2011, vol. 519(13), pp. 2677–2696. https://doi.org/10.1002/cne.22646

  139. Belekhova, M.G., Kenigfest, N.B., Vesselkin, N.P., Rio, J.-P., Repérant, J., and Ward, R., Evolutonary significance of different neurochemical organization of the internal and external regions of auditory centers in the reptilian brain: an immunocytochemical and reduced NADPH-diaphorase histochemical study in turtles, Brain Res., 2002, vol. 925(1), pp. 100–106. https://doi.org/10.1016/s0006-8993(01)03255-3

  140. Yan, K., Tang, Y.-Z., and Carr, C.E., Calcium-binding protein immunoreactivity characterizes the auditory system of Gekko gecko, J. Comp. Neurol., 2010, vol. 518(17), pp. 3409–3426. https://doi.org/10.1002/cne.22428

  141. Chudinova, T.V., Belekhova, M.G., Tostivint, E., Rio, J.-P., Ward, R., and Kenigfest, N.B., Differences in CB- and PV-chemospecificity in the centres of the ascending auditory pathway of turtles revealed by double immunofluorescence labeling, Brain Res., 2012, vol. 1473, pp. 87–103. https://doi.org/10.1016/j.brainres.2012.07.022

  142. Lanuza, E., Belekhova, M.G., Martinez-Marcos, A., Font, C., and Martinez-Garcia, F., Identification of the basolateral amygdale; an anatomical investigation of afferents to the posterior dorsal ventricular ridge of the lizard Podarcis hispanica, Eur. J. Neurosci., 1998, vol. 10(11), pp. 3517–3574. https://doi.org/10.1046/j.1460-9568.1998.00363.x

  143. Chkheidze, D.D. and Belekhova, M.G., Projections of olfactory bulbs and non-olfactory telencephalic structures in amygdaloid complex of the turtle Testudo horsfieldi: a study using anterograde tracer technique, J. Evol. Bioch. Physiol., 2005, vol. 41(5), pp. 561– 569.

  144. Medina, L., Bupesh, M., and Abellan, A., Contribution of genoarchitecture to understanding forebrain evolution and development with particular emphasis on the amygdale, Brain Behav. Evol., 2011, vol. 78(3): 216–236. https://doi.org/10.1159/000330056

  145. Piniak, W.E.D., Mann, D.A., Harms, C.A., Jones, T.T., Eckert, S.A., Hearing in the juvenile green sea turtle (Chelonia midas): a comparison under water and aerial hearing using auditory evoked potentials, PLoS One, 2016, vol. 11, e0159711. https://doi.org/10.1371/journal.pone.0159711

  146. Higgs, D.M., Brittan-Powell, E.F., Soares, D., Sonza, M.J., Carr, C.E., et al., Amphibious auditory responses of the American alligator (Alligator mississipiensis), J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol., 2002, vol. 188(3), pp. 217–223. https://doi.org/10.1007/s00359-002-0296-8

  147. Brittan-Powell, E.F., Cristensen-Dalsgaard, J., Tang, J., Carr, C.E., and Dooling, R.J., The auditory brainstem responses in two lizard species, Acoust. Soc. Am., 2010, vol. 128(2), pp. 787–792. https://dx.doi.org/10.1121%2F1.3458813

  148. Vergene, A., Pritz, M.B., and Mathevon, N., Acoustic communication in crocodilians: from behavior to brain, Biol. Rev. Camb. Philos. Soc., 2009, vol. 84(3), pp. 391–411. https://doi.org/10.1111/j.1469-185x.2009.00079.x

  149. Behroozi, M., Billings, B.K., Helluy, X., Manger, P.R., Güntürkün, O., and Ströckens, F., Functional MRI in the Nile crocodile: a new avenue for evolutionary neurobiology, Proc. Biol. Sci., 2018, vol. 285(1877). https://doi.org/10.1098/rspb.2018.0178

  150. Huang, Y.F., Zhang, J.Y., Xi, C., Zeng, S.J., Zhang, X.W., and Zuo, M.X., Germinal sites and migrating routes of cells in the mesencephalic and diencephalic auditory areas in the African clawed frog (Xenopus laevis), Brain Res., 2011, vol. 1373, pp. 67–78. https://doi.org/10.1016/j.brainres.2010.12.026

  151. Moreno, N. and Gonzalez, A., Localization and connectivity of the lateral amygdala in anuran amphibians, J. Comp. Neurol., 2004, vol. 479(2), pp. 130–148. https://doi.org/10.1002/cne.20298

  152. Laberge, F. and Roth, G., Organization of the sensory input to the telencephalon in the fire-belled toad, Bombina orientalis, J. Anat., 2007, vol. 502(1), pp. 55–78. https://doi.org/10.1002/cne.21297

  153. Hall, I.C., Ballagh, I.H., and Kelley, D.B., The Xenopus amygdale mediates appropriate vocal communicative signals, J. Neurosci., 2013, vol. 33(36), pp. 14534–14548. https://doi.org/10.1523/JNEUROSCI.1190-13.2013

  154. Paddington, M.H., Daneri, M.F., Papini, M.R., and Muzio, R.N., Telencephalic neural activation following passive avoidance learning in a terrestrial toad, Brain Behav. Res., 2016, vol. 315, pp. 75–82. https://doi.org/10.1016/j.bbr.2016.08.003

  155. Slutsky, D.A., Manger, P.R., and Kubitzer, L., Multiple somatosensory areas in parietal cortex of the California grand squirrel (Spermoohilus beecheyll), J. Comp. Neurol., 2000, vol. 416(4), pp. 521–539. https://doi.org/10.1002/(sici)1096-9861(20000124)416:4%3C521::aid-cne8%3E3.0.co;2-#

  156. Winer, J.A., The human medial geniculate body, Hear Res., 1984, vol. 15(3), pp. 225–247. https://doi.org/10.1016/0378-5955(84)90031-5

  157. Kaas, J.H., Hackett, T.A., and Tramo, M.J., Auditory processing in primates cerebral cortex, Curr. Opin. Neurobiol., 1999, vol. 9(2), pp. 164–170. https://doi.org/10.1016/s0959-4388(99)80022-1

  158. Striedter, J.F., Principles of Brain Evolution, University California Press, Irvine, 2005.

  159. Kaas, J.H., Reconstructing the areal organization of the neocortex of the first mammals, Brain Behav. Evol., 2011, vol. 78(1), pp. 7–21. https://doi.org/10.1159/000327316

  160. Krubitzer, L. and Hoffman, K.J., Arealization of the neocortex in mammals: genetic and epigenetic contributions, Brain Behav. Evol., 2000, vol. 55(6), pp. 201–208. https://doi.org/10.1159/000006667

  161. Krubitzer, L., The magnificent compromise: cortical field evolution in mammals, Neuron, 2007, vol. 56 (2), pp. 201–208. 2007. https://doi.org/10.1016/j.neuron.2007.10.002

  162. Karten, H.J., Vertebrate brain and evolutionary connectomics: on the origins of mammalian “neocortex”, Phil. Trans. Roy. Soc. Lond. Biol. Sci., 2015, vol. 370(1684). https://doi.org/10.1098/rstb.2015.0060

  163. Le Doux, J.E., Rethinking the emotional brain, Neuron, 2012a, vol. 73(4), pp. 653–676. https://doi.org/10.1016/j.neuron.2012.02.004

  164. Le Doux, J.E., Evolution of human emotion: a view through the fear, Progr. Brain. Res., 2012b, vol. 195, pp. 431–442. https://dx.doi.org/10.1016%2FB978-0-444-53860-4.00021-0

  165. Martinez-Garcia, F. and Lanuza, E., Evolution of the vertebrate survival circuits, Curr. Opin. Behav. Sci., 2018, vol. 24, pp. 113–123. https://doi.org/10.1016/j.cobeha.2018.06.012

  166. Butler, A.B., The evolution of the dorsal thalamus of jawed vertebrates, including mammals: cladistic analysis and a new hypothesis, Brain Res. Rev., 1994, vol. 19(1), pp. 29–65. https://doi.org/10.1016/0165-0173(94)90003-5

  167. Butler, A.B. and Hodos, W., Comparative Vertebrate Neuroanatomy. Evolution and Adaptation, 2nd edition, Hoboken, New Jersey, 2005.

  168. Puelles, L., Thoughts on the development structure and evolution of the mammalian and avian telencephalic pallium, Phil. Trans. R. Soc. B, 2001, vol. 156(1414), pp. 1583–1598. https://doi.org/10.1098/rstb.2001.0973

  169. Wild, J.M. and Krützfeldt, N.O.E., Neocortical-like organization of avian auditory cortex, Brain Behav. Evol., 2010, vol. 76(2), pp. 89–92. https://doi.org/10.1159/000320215

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This work was supported by the State funding (reg. no. АААА–A18-118012290372-0, direction 5 “Neurophysiological mechanisms of the regulation of functions and their evolution”).

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Belekhova, M.G., Kenigfest, N.B. & Chmykhova, N.M. Evolutionary Formation and Functional Significance of the Core–Belt Pattern of Neural Organization of Rostral Auditory Centers in Vertebrates. J Evol Biochem Phys 56, 283–303 (2020). https://doi.org/10.1134/S0022093020040018

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