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Role of von Economo and fork neurons in the evolution of vocal learning

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Abstract

The present review presents a new and feasible assumption in the comparative neurobiology of vocal production learning that underpins human speech. Vocal learning, the competence of modulating acoustic sounds or imitating novel sounds, is a requisite requirement of human spoken language and is considered a major innovation for the evolutionary origin of human verbal communication. Having numerous examples of impaired language in many neurodegenerative diseases caused by brain injury, until now our knowledge about the underlying neural procedure for verbal communication is inadequate. This capacity is restricted in a few distantly related groups of mammals and birds like humans, elephants, cetaceans, pinnipeds, bats, a few primates, and three genera of birds—parrots, songbirds, and hummingbirds. Astonishingly atypical neuronal type-spindle-shaped bipolar projection neurons-the von Economo neurons (VENs) and fork neurons are also detected in V layer of the anterior cingulate cortex (ACC) and frontoinsular cortex (FI) of identical groups of mammals and even in some telencephalic nuclei of bird species (parrots) that do not have a neocortex. Review evaluations speculate that capability of vocal imitation and learning is the shared feature of all animals containing VENs and probably fork neurons. The communication systems and their neural architecture in nonhuman animals have been reviewed and their significance has been discussed. The present review is intended to develop a new speculation regarding the neural mechanisms of vocalizition in nonhuman animals and human language.

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Fig. 1
Fig. 2

(Source of the figs. Srivastava & Shrivastava, (Von Economo neurons in the Indian green Ringneck Parrot (Psittacula krameri)): possible role in vocal learning. Aus. Anat. 4, 1–10). 2017 (Presence of VENs and fork neurons in bird brain has been studied in my lab)

Fig. 3

(Source of the figs. Srivastava & Shrivastava, (von Economo neurons in the Indian green Ringneck Parrot (Psittacula krameri)): possible role in vocal learning. Aus. Anat. 4, 1–10). 2017 (Presence of VENs and fork neurons in bird brain has been studied in my lab)

Fig. 4

(Source of the figs. Srivastava & Shrivastava, (Von Economo neurons in the Indian green Ringneck Parrot (Psittacula krameri)): possible role in vocal learning. Aus. Anat. 4, 1–10). 2017 (Presence of VENs and fork neurons in bird brain has been studied in my lab)

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References

  1. Coude G, Ferrari PF, Rodà F., Maranesi M, Borell, E, Veroni V, et al.(2011) Neurons controlling voluntary vocalization in the macaque ventral premotor cortex.PloS One, 6, e26822. doi:https://doi.org/10.1371/journal.pone.0026822

  2. Macedonia JM. The vocal repertoire of the ring-tailed lemur (Lemur catta). (1993) Folia Primatologica. 61:186-217.

    Article  CAS  Google Scholar 

  3. Pouw W, Hostetter AB (2016) Gesture as predictive action. Reti Saperi Linguaggi 3:57–80.

    Google Scholar 

  4. Janik, V.M., Slater, PJB. (1997) Vocal learning in mammals. Adv. Study. behave 26: 59-99..

    Article  Google Scholar 

  5. Poole JH, Tyack PL, Stoeger-Horwth AS (2005) Watwood S. Animal behavior. Elephants are capable of vocal learning. Nature 434: 455-456

    Article  CAS  PubMed  Google Scholar 

  6. Boughman JW. (1998) Vocal learning by greater spear-nosed bats. Proc R Soc B 265: 227-233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Reynolds J E, and Odell K O (1991).Manatees and Dugongs Facts on File, (Inc., New York, USA

  8. Weary D M, Fraser D (1997) Vocal response of piglets to weaning: effect of piglet age. Applied Ani Behav Sci. 54: 153-160.

    Article  Google Scholar 

  9. Vannoni E, McElligott A G, (2008). Low-frequency groans indicate larger and more dominant fallow deer (Dama dama) males. PLoS One, 3,

  10. Kirshenbaum A, Ilany A, Blaustein L, Geffen E, (2012) Syntactic structure and geographical dialects in the songs of male rock hyraxes. Proceedings of the Royal Society B: 1–8.

  11. von Economo C, Koskinas GN. Die (1925) Cytoarchitektonik der Hirnrinde des Erwachsenen Menschen. Berlin (Germany): Springer;

    Google Scholar 

  12. Nimchinsky E.A, Gilissen E, Allman J, Perl D, Erwin J, Hof P A (1999) neuronal morphological type unique to humans and great apes. Proc Nat Acad Sci USA 96: 5268–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Allman JM, Tetreault NA, Hakeem AY, Manaye K F, Semendeferi K, Erwin JM, Park S, Goubert V, Hof P R, (2010). The Von-Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct. 214: 495-517

    Article  PubMed  Google Scholar 

  14. Rose M. Die inselrinde des menschen und der tiere. (1928) Journal fur Psychologie und Neurologie.;37:468–624.

    Google Scholar 

  15. Evrard HC, Forro T, Logothetis N K. (2012) Von Economo neurons in the anterior insula of the macaque monkey. Neuron. 74: 482-489

    Article  CAS  PubMed  Google Scholar 

  16. Butti et al. (2014) The Cerebral Cortex of the Pygmy Hippopotamus, Hexaprotodon liberiensis Cetartiodactyla, Hippopotamidae): MRI, Cytoarchitecture, and Neuronal Morphology Anat Rec. 297: 670–700

    Google Scholar 

  17. Butti C, Sherwood C C, Hakeem AY, Allman JM, and Hof P R (2009) Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans. J. Com. Neurol. 515: 243-259

    Article  Google Scholar 

  18. Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR Allman JM (2009) Von Economo neurons in the elephant brain. Ana. Rec. 292: 242-248.

    Article  Google Scholar 

  19. Raghanti MA, Spurlock LB,Treichler FR, Weigel SE, Stimmelmayr R, Butti C Thewissen JG, Hof PR (2015) An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls. Brain. Struct Funct. 220: 2303-2314

    Article  PubMed  Google Scholar 

  20. Hof PR, and Gucht V D (2007) Structure of the cerebral cortex of the humpback whale,MegapteranovaeangliaeCetacea, Mysticeti, Balaenopteridae). Anat Rec (Hoboken) 290: 1-31.

    Article  PubMed  Google Scholar 

  21. Butti C., Hof P. R. (2010). The insular cortex: a comparative perspective. Brain Struct. Funct. 214: 477–493 https://doi.org/10.1007/s00429-010-0264

    Article  PubMed  Google Scholar 

  22. Ngowyang G. Beschreibung einer Art von Spezialzellen in der Inselrinde—zugleich Bemerkungen über die v. Economoschen Spezialzellen. (1932 ) J Psychol Neurol. 44:671–674.

  23. Taniguchi M, Iwahashi M, Oka Y, Tiong SYX, Sato M (2022) Fezf2-positive fork cell-like neurons in the mouse insular cortex. PLoS ONE 17(9): e0274170. https://doi.org/ https://doi.org/10.1371/journal . pone.0274170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. .Pepperberg I. (1999a) The Alex Studies: Cognitive and Communicative Abilities of Grey Parrots. 96–167, ( Cambridge, Massachusetts, Harvard Univ. Press

  25. Jarvis E D (2004), learned bird songs and the neurobiology of human languages. Ann. NY Acad sci 016: 749-777.

    Article  Google Scholar 

  26. Doupe A J, & Kuhl P K.(1999) Birdsong and human speech: Common themes and mechanisms. Annual Review of Neuroscience, 22: 567–631.

    Article  CAS  PubMed  Google Scholar 

  27. Bottjer SW, Halsema KA, Brown SA, Miesner EA (1989) Axonal connections of a forebrain nucleus involved vocal learning in zebra finches. J Comp Neurol 279: 312-326.

    Article  CAS  PubMed  Google Scholar 

  28. Jarvis ED, Mello CV (2000) Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419: 1–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Chakraborty M, Walløe S, Nedergaar S, Fridel E E, Dabelsteen T, Pakkenberg B, Bertelsen M F, Dorrestein G M, Brauth S E, Durand, SE, Jarvis E D. (2015) Core and Shell Song Systems Unique to the Parrot Brain.PLoS.ONE10(6):e0118496. https://doi.org/10.1371/journal.pone.0118496 .

  30. Srivastava S, Shrivastava S, (2017). Von Economo neurons in Indian green Ring neck Parrot (Psittacula krameri)): possible role in vocal learning. Aus. J Anat. 4: 1-10.

    Google Scholar 

  31. Gahr M (2000) Neural song control system of hummingbirds: comparison to swifts, vocal learning (Songbirds) and non-learning (Sub oscines) passerines, and vocal learning (Budgerigars) and non-learning (Dove, owl, gull, quail, chicken) non-passerines. J Comp Neurol. 426: 182–196.

    Article  CAS  PubMed  Google Scholar 

  32. Honig, W.K., (1978). Studies of working memory in the pigeon. In: (SH Hulse & W K Honig Eds.) Cognitive processes in animal behavior 211– 248. (New York: Hillsdale.1978)

  33. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, Dearmond, SJ, (2006) Early frontotemporal dementia targets neurons unique to apes and humans. Ann Neurol 60: 660–667.

    Article  PubMed  Google Scholar 

  34. Kaufman JA, Paul LK, Manaye KF, Granstedt AE, Hof PR, Allman JM (2008) Selective reduction of Von Economo neuron number in agenesis of the corpus callosum. Acta Neuropathologica. 116: 479–489.

    Article  PubMed  Google Scholar 

  35. Allman JM, Watson K, Tetreault N, Hakeem A, (2005) Intuition, and autism: A possible role for Von Economo neurons Trends Cogn sci. 9: 367–373.

  36. Santos M, Uppal N, Butti C, Wicinski B, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR. (2011) Von Economo neurons in autism: a stereological study of the frontoinsular cortex in children. Brain Res 1380: 7.

    Article  Google Scholar 

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Acknowledgements

We thank Dr. Sudhi Srivastava, (Assistant Professor, Dept. of Zoology, C M P Degree College University of Allahabad U.P. India) for her constructive involvement to prepare slides of Parrot brains to study VENs. We thank Dr. Vinay Khanna, principal scientist IITR, Lucknow U P India for his very gentle support in the photography of neurons.

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  1. Department of Zoology, Kashi Naresh Government Postgraduate College, Gyanpur, Bhadohi, India

    Shubha Srivastava

  2. Prayagraj, India

    Shubha Srivastava

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Correspondence to Shubha Srivastava.

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Srivastava, S. Role of von Economo and fork neurons in the evolution of vocal learning. Neurosci Behav Physi 53, 695–706 (2023). https://doi.org/10.1007/s11055-022-01341-0

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