A unique cellular scaling rule in the avian auditory system

Brain Structure and Function

Volumn 221, Issue 5, 2016, Pages 2675-2693

  Corfield, Jeremy R ^a,b   Long, Brendan ^a   Krilow, Justin M ^a   Wylie, Douglas R ^b   Iwaniuk, Andrew N ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

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

Indexed keywords

ALLOMETRY; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY SYSTEM; BIRD; BRAIN SIZE; BRAIN STEM; CELL COUNT; CELL DENSITY; GALLIFORMES; HAIR CELL; MAMMAL; NERVE CELL; NONHUMAN; PERCEPTION; PRIMATE; PRIORITY JOURNAL; SOUND; ANIMAL; CELL SIZE; COCHLEAR NUCLEUS; CYTOLOGY; INNER EAR; SPECIES DIFFERENCE;

ANIMALS; AUDITORY PATHWAYS; CELL COUNT; CELL SIZE; COCHLEAR NUCLEUS; EAR, INNER; GALLIFORMES; NEURONS; SPECIES SPECIFICITY;

EID: 84929678409     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1064-1     Document Type: Article

References (108)

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