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A unique cellular scaling rule in the avian auditory system

Abstract

Although it is clear that neural structures scale with body size, the mechanisms of this relationship are not well understood. Several recent studies have shown that the relationship between neuron numbers and brain (or brain region) size are not only different across mammalian orders, but also across auditory and visual regions within the same brains. Among birds, similar cellular scaling rules have not been examined in any detail. Here, we examine the scaling of auditory structures in birds and show that the scaling rules that have been established in the mammalian auditory pathway do not necessarily apply to birds. In galliforms, neuronal densities decrease with increasing brain size, suggesting that auditory brainstem structures increase in size faster than neurons are added; smaller brains have relatively more neurons than larger brains. The cellular scaling rules that apply to auditory brainstem structures in galliforms are, therefore, different to that found in primate auditory pathway. It is likely that the factors driving this difference are associated with the anatomical specializations required for sound perception in birds, although there is a decoupling of neuron numbers in brain structures and hair cell numbers in the basilar papilla. This study provides significant insight into the allometric scaling of neural structures in birds and improves our understanding of the rules that govern neural scaling across vertebrates.

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References

  1. Barton RA (1998) Visual specialization and brain evolution in primates. Proc R Soc Lond B 265:1933–1937

  2. Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058

  3. Cajal SR (1908) Les ganlions terminaux du nerf acoustique des oiseaux. Trab Inst Cajal Invest Biol 6:195–225

  4. Carr CE, Boudreau RE (1993) Organization of the nucleus magnocellularis and the nucleus laminaris in the barn owl: encoding and measuring interaural time differences. J Comp Neurol 334:337–355

  5. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brainstem of the barn owl. J Neurosci 10:3227–3246

  6. Carr CE, Soares D (2002) Evolutionary convergence and shared computational principles in the auditory system. Brain Behav Evol 59:294–311

  7. Chalfin BP, Cheung DT, Muniz JAPC, de Lima Silveira LC, Finlay BL (2007) Scaling of neuron number and volume of the pulvinar complex in New World primates: comparisons with humans, other primates, and mammals. J Comp Neurol 504:265–274

  8. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272–274

  9. Cobb S (1964) A comparison of the size of an auditory nucleus (n. mesensephalicus lateralis, pars dorsalis) with the size of the optic lobe in twenty seven species of birds. J Comp Neurol 122:271–279

  10. Cohen YE, Miller GL, Knudsen EI (1998) Forebrain pathway for auditory space processing in the barn owl. J Neurophysiol 79:891–902

  11. Collins CE, Leitch DB, Wong P, Kaas JH, Herculano-Houzel S (2013) Faster scaling of visual neurons in cortical areas relative to subcortical structures in non-human primate brains. Brain Struct Funct 218:805–816

  12. Conlee JW, Parks TN (1986) Origin of ascending auditory projections to the nucleus mesencephalicus lateralis pars dorsalis in the chicken. Brain Res 367:96–113

  13. Corfield JR, Kubke MF, Parsons S, Wild JM, Koppl C (2011) Evidence for an auditory fovea in the New Zealand kiwi (Apteryx mantelli). PLoS One 6(8):e23771. doi:10.1371/journal.pone.0023771

  14. Corfield JR, Kubke MF, Parsons S, Koppl C (2012a) Inner-ear morphology of the New Zealand kiwi (Apteryx mantelli) suggests high-frequency specialization. J Assoc Res Otolaryngol 13:629–639

  15. Corfield JR, Wild JM, Parsons S, Kubke MF (2012b) Morphometric analysis of telencephalic structure in a variety of Neognath and Paleognath bird species reveals regional differences associated with specific behavioral traits. Brain Behav Evol 80:181–195

  16. Corfield JR, Krilow JM, Vande Ligt MN, Iwaniuk AN (2013a) A quantitative morphological analysis of the inner ear of galliform birds. Hear Res 304:111–127

  17. Corfield JR, Kubke MF, Köppl C (2013b) Emu and kiwi: the ear and hearing in Paleognathous birds. In: Manley GA, Köppl C, Popper A, Fay RR (eds) Insights from comparative hearing research. Springer handbook in auditory research. Springer, New York

  18. Craigie EH (1930) Studies on the brain of the kiwi (Apteryx australis). J Comp Neurol 49:223–357

  19. de Winter W, Oxnard CE (2001) Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409:710–714

  20. Dooling RJ, Lohr B, Dent ML (2000) Hearing in birds and reptiles. In: Dooling RJ, Popper A, Fay R (eds) Comparative hearing: birds and mammals. Springer handbook of auditory research. Springer, New York, pp 308–359

  21. Dunning JB (2007) CRC handbook of avian body masses, 2nd edn. CRC Press, Boca Raton

  22. Durand SE, Tepper JM, Cheng M-F (1992) The shell region of the nucleus ovoidalis: a subdivision of the avian auditory thalamus. J Comp Neurol 323:495–518

  23. Dyson ML, Klump GM, Gauger B (1998) Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J Comp Physiol 182:695–702

  24. Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13:1124–1138

  25. Elston GN, Manger P (2014) Pyramidal cells in V1 of African rodents are bigger more branched and more spiny than those in primates. Front Neuroanat. doi:10.3389/fnana.2014.00004

  26. Finlay BK, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584

  27. Frahm HD, Rehkamper G (1998) Volumetric comparison of auditory brain nuclei in ear-tufted Araucanas with those in other chicken breeds. J Hirnforsch 39:37–44

  28. Funabiki K, Koyano K, Ohmori H (1998) The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J Physiol 508:851–869

  29. Gleich O, Manley GA (2000) The hearing organ of birds and crocodilia. In: Dooling RJ, Fay R, Popper A (eds) Comparative hearing: birds and reptiles. Springer, New York, pp 70–138

  30. Gleich O, Fischer FP, Köppl C, Manley GA (2004) Hearing organ evolution and specialization: Archosaurs. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 224–255

  31. Gleich O, Dooling RJ, Manley GA (2005) Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenschaften 92:595–598

  32. Gullion GW (1965) Improvements in the methods for trapping and marking ruffed grouse. J Wild Manag 29:109–116

  33. Gundersen HJG, Jensen EBV, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology—reconsidered. J Microsc 193:199–211

  34. Gutierrez-Ibanez C, Iwaniuk AN, Wylie DR (2011) Relative size of auditory pathways in symmetrically and asymmetrically eared owls. Brain Behav Evol 78:286–301

  35. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

  36. Hausler UH, Sullivan WE, Soares D, Carr CE (1999) A morphological study of the cochlear nuclei of the pigeon (Columba livia). Brain Behav Evol 54:290–302

  37. Herculano-Houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 3:31

  38. Herculano-Houzel S, Lent R (2005) Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci 25:2518–2521

  39. Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138–12143

  40. Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104:3562–3567

  41. Herculano-Houzel S, Avelino-de-Souza K, Neves K, Porfirio J, Messeder D, Feijo LM, Maldonado J, Manger PR (2014a) The elephant brain in numbers. Front Neuroanat. doi:10.3389/Fnana.2014.00046

  42. Herculano-Houzel S, Manger PR, Kaas JH (2014b) Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size. Front Neuroanat. doi:10.3389/Fnana.2014.00077

  43. Hill EM, Koay G, Heffner RS, Heffner HE (2014) Audiogram of the chicken (Gallus gallus domesticus) from 2 to 9 kHz. J Comp Physiol A. doi:10.1007/s00359-014-0929-8

  44. Hotta T (1971) Unit responses from the nucleus angularis in the pigeon’s medulla. Comp Biochem Physiol 40A:415–424

  45. Howard CV, Reed MG (2005) Unbiased stereology. Three-dimensional measurement in microscopy. Springer, New York

  46. Husband S, Shimizu T (2001) Evolution of the avian visual system. In: Cook RG (ed) Avian visual cognition. Tufts University, Medford

  47. Hyson RL (2005) The analysis of interaural time differences in the chick brain stem. Physiol Behav 86:297–305

  48. Hyson RL, Overholt EM, Rubel EW (1989) Spatial summation for coding interaural time disparities in nucleus laminaris of the chick. J Comp Neurol 12:34–35

  49. Iwaniuk AN, Clayton DH, Wylie DRW (2006) Echolocation, vocal learning, auditory localization and the relative size of the avian auditory midbrain nucleus (MLd). Behav Brain Res 167:305–317

  50. Iwaniuk AN, Heesy CP, Hall MI, Wylie DR (2008) Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds. J Comp Physiol A 194:267–282

  51. Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psych 41:35–39

  52. Jerison HJ (1973) Evolution of the brain and intelligence. Academic Press, New York

  53. Jhaveri S, Morest DK (1982) Neuronal architecture in nucleus magnocellularis of the chicken with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7:809–836

  54. Karten HJ (1967) The organization of the ascending auditory pathway in the pigeon (Columba livia). I. Diencephalic projections of the inferior colliculus (nucleus mesencephali lateralis, pars dorsalis). Brain Res 6:409–427

  55. Karten HJ, Hodos W (1967) A stereotaxic atlas of the brain of the pigeon. Johns Hopkins, Baltimore

  56. Kaskan PM, Franco ECS, Yamada ES, de Lima Silveira LC, Darlington RB, Finlay BL (2005) Peripheral variability and central constancy in mammalian visual system evolution. Proc R Soc Lond B 272:91–100

  57. Konishi M (1973) How the owl tracks its prey. Am Sci 61:414–424

  58. Köppl C (2001) Tonotopic projections of the auditory nerve to the cochlear nucleus angularis in the barn owl. J Assoc Res Otolaryngol 2:41–53

  59. Köppl C, Carr CE (1997) Low-frequency pathway in the barn owl’s auditory brainstem. J Comp Neurol 378:265–282

  60. Köppl C, Carr CE (2003) Computational diversity in the cochlear nucleus angularis of the barn owl. J Neurophysiol 89:2313–2329

  61. Köppl C, Gleich O, Manley GA (1993) An auditory fovea in the barn owl cochlea. J Comp Physiol A 171:695–704

  62. Köppl C, Wegscheider A, Gleich O, Manley GA (2000) A quantitative study of cochlear afferent axons in birds. Hear Res 139:123–143

  63. Kuba H, Yamada R, Fukui I, Ohmori H (2005) Tonotopic specialization of auditory coincidence detection in nucleus laminaris of the chick. J Neurosci 25:1924–1934

  64. Kubke MF, Carr CE (2006) Morphological variation in the nucleus laminaris of birds. Intern J Comp Psychol 19:83–97

  65. Kubke MF, Massoglia DP, Carr CE (2004) Bigger brains or bigger nuclei? Regulating the size of auditory structures in birds. Brain Behav Evol 63:169–180

  66. Kuenzel WJ, Masson M (1988) A stereotaxic atlas of the brain of the chick (Gallus Domesticus). The Johns Hopkins University Press, Baltimore

  67. Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246

  68. Lippe WR (1991) Reduction and recovery of neuronal size in the cochlear nucleus of the chicken following aminoglycoside intoxication. Hear Res 51:193–202

  69. Logerot P, Krutzfeldt NO, Wild JM, Kubke MF (2011) Subdivisions of the auditory midbrain (n. mesencephalicus lateralis, pars dorsalis) in zebra finches using calcium-binding protein immunocytochemistry. PLoS One 6(6):e20686. doi:10.1371/journal.pone.0020686

  70. MacLeod KM, Soares D, Carr CE (2006) Interaural timing difference circuits in the auditory brainstem of the emu (Dromaius novaehollandiae). J Comp Neurol 495:185–201

  71. Maiorana VA, Schleidt WM (1972) The auditory sensitivity of the turkey. J Aud Res 12:203–207

  72. Marin F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738

  73. Moiseff A (1989) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164:637–644

  74. Neves K, Ferreira FM, Tovar-Moll F, Gravett N, Bennett NC, Kaswera C, Gilissen E, Manger PR, Herculano-Houzel S (2014) Cellular scaling rules for the brain of afrotherians. Front Neuroanat 8:1–13

  75. Niemiec AJ, Raphael Y, Moody DB (1994) Return of auditory function following structural regeneration after acoustic trauma: behavioral measures from quail. Hear Res 79:1–16

  76. Parks TN, Rubel EW (1975) Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J Comp Neurol 164:435–448

  77. Parks TN, Rubel EW (1978) Organization and development of the brainstem auditory nuclei of the chicken: primary afferent projections. J Comp Neurol 180:435–448

  78. Payne RS (1971) Acoustic location of prey by barn owls (Tyto alba). J Exp Biol 54:535–573

  79. Puelles L, Robles C, Martinez-de-la-Torre M, Martinez S (1994) New subdivision schema for the avian torus semicircularis: neurochemical maps in the chick. J Comp Neurol 340:98–125

  80. Puelles L, Martinez de la Torre M, Paxinos G, Watson C, Martinez S (2007) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies. Academic Press, Waltham

  81. Rasband WS (1997) ImageJ, U. S. National Institutes of Health. Bethesda, Maryland, USA. http://imagej.nih.gov/ij/

  82. Ribeiro PF, Manger PR, Catania KC, Kaas JH, Herculano-Houzel S (2014) Greater addition of neurons to the olfactory bulb than to the cerebral cortex of eulipotyphlans but not rodents, afrotherians or primates. Front Neuroanat 8:1–12

  83. Rubel EW, Parks TN (1975) Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of N. magnocellularis and N. laminaris. J Comp Neurol 164:411–434

  84. Rubel EW, Smith DJ, Miller LC (1976) Organization and development of brain stem auditory nuclei of the chicken: ontogeny of n. magnocellularis and n. laminaris. J Comp Neurol 166:469–490

  85. Sachs MB, Sinnott JM (1978) Responses to tones of single cells in nucleus magnocellularis and nucleus angularis of the redwing blackbird (Agelaius phoeniceus). J Comp Physiol 126:347–361

  86. Sarko DK, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S (2009) Cellular scaling rules of insectivore brains. Front Neuroanat 3:8. doi:10.3389/neuro.05.008.2009

  87. Smith DJ, Rubel EW (1979) Organization and development of brain stem auditory nuclei of the chicken: dendritic gradients in nucleus laminaris. J Comp Neurol 186:213–239

  88. Soares D, Carr CE (2001) The cytoarchitecture of the nucleus angularis of the barn owl (Tyto alba). J Comp Neurol 429:192–205

  89. Stevens CF (2001) An evolutionary scaling law for the primate visual system and its basis in cortical function. Nature 411:193–195

  90. Striedter GF (2005) Principles of brain evolution. Sinauer, Sunderland

  91. Sullivan WE (1985) Classification of response patterns in cochlear nucleus of barn owl: correlation with functional response properties. J Neurophysiol 53:201–216

  92. Sullivan WE, Konishi M (1984) Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J Neurosci 4:1787–1799

  93. Sullivan WE, Konishi M (1986) Neural map of interaural phase difference in the owl’s brainstem. Proc Natl Acad Sci USA 83:8400–8404

  94. Takahashi T, Konishi M (1988a) Projections of nucleus angularis and nucleus laminaris to the lateral lemniscal nuclear complex of the barn owl. J Comp Neurol 274:212–238

  95. Takahashi T, Konishi M (1988b) Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J Comp Neurol 274:190–211

  96. Takahashi T, Moiseff A, Konishi M (1984) Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4:1781–1786

  97. Timmermans S, Lefebvre L, Boire D, Basu P (2000) Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203

  98. Van Dijk T (1973) A comparative study of hearing in owls of the family strigidae. Neth J Zool 23:131–167

  99. Wagner H, Gunturkun O, Nieder B (2003) Anatomical markers for the subdivisions of the barn owl’s inferior-collicular complex and adjacent peri- and subventricular structures. J Comp Neurol 465:145–159

  100. Walsh SA, Barrett PM, Milner AC, Manley G, Witmer LM (2009) Inner ear anatomy is a proxy for deducing auditory capability and behaviour in reptiles and birds. Proc R Soc Lond B 276:1355–1360

  101. Wang N, Kimball RT, Braun EL, Liang B, Zhang Z (2013) Assessing phylogenetic relationships among galliformes: a multigene phylogeny with expanded taxon sampling in Phasianidae. PLoS One 8(5):e64312. doi:10.1371/journal.pone.0064312

  102. Warchol ME, Dallos P (1990) Neural coding in the chick cochlear nucleus. J Comp Physiol A 166:721–734

  103. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497

  104. Wild JM (1987) Nuclei of the lateral lemniscus project directly to the thalamic auditory nuclei in the pigeon. Brain Res 408:303–307

  105. Wild JM (1995) Convergence of somatosensory and auditory projections in the avian torus semicircularis, including the central auditory nucleus. J Comp Neurol 358:465–486

  106. Williams RW, Herrup K (1988) The control of neuron number. Annu Rev Neurosci 11:423–453

  107. Winter P (1963) Verglecende qualitative und quantitative untersuchungen an der horbahn von vogeln. Z Morphol Anthropol 52:365–400

  108. Wong P, Peebles JK, Asplund CL, Collins CE, Herculano-Houzel S, Kaas JH (2013) Faster scaling of auditory neurons in cortical areas relative to subcortical structures in primate brains. Brain Behav Evol 81:209–218

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Acknowledgments

We would like to thank all of the hunters and falconers that assisted us in obtaining specimens in Alberta and New Zealand, in particular, Brent Davidson, Lynn Oliphant and Udo Hannebaum. We thank also the two anonymous reviewers for their constructive feedback on the manuscript. Funding for this study was provided by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (372237) and Accelerator Supplement (380284-2009) to ANI and NSERC (446013) grants to DRW.

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The authors declare that there are no conflicts of interests.

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Correspondence to Jeremy R. Corfield.

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Corfield, J.R., Long, B., Krilow, J.M. et al. A unique cellular scaling rule in the avian auditory system. Brain Struct Funct 221, 2675–2693 (2016). https://doi.org/10.1007/s00429-015-1064-1

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Keywords

  • Nucleus magnocellularis
  • Nucleus laminaris
  • Nucleus angularis
  • Neural scaling
  • Comparative neuroanatomy
  • Allometry