Distribution of substance P reveals a novel subdivision in the hippocampus of parasitic South American cowbirds

Journal of Comparative Neurology

Volumn 496, Issue 5, 2006, Pages 610-626

  Nair Roberts, Radha G ^a   Erichsen, Jonathan T ^b   Reboreda, Juan C ^c   Kacelnik, Alex ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Avian brain; Brood parasitism; Lateral mammillary nucleus; Spatial memory

Indexed keywords

SUBSTANCE P;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BAY WINGED COWBIRD; BIRD; BRAIN REGION; BREEDING; BROOD PARASITISM; CREAMING COWBIRD; DENTATE GYRUS; DIENCEPHALON; ELECTRON MICROSCOPY; FEMALE; GOLGI COMPLEX; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATERAL MAMMILLARY NUCLEUS; MALE; MESENCEPHALON; MICROSCOPY; NERVE PROJECTION; NESTING; NONHUMAN; PIGEON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGRESSION ANALYSIS; SEASONAL VARIATION; SEX DIFFERENCE; SEXUAL BEHAVIOR; SHINY COWBIRD; SONGBIRD; SOUTH AMERICAN COWBIRD; SPATIAL MEMORY; SPECIES COMPARISON; SUBICULUM; SUPRAMAMMILLARY NUCLEUS; SYMPATRY; SYNAPSE; TELENCEPHALON; ULTRASTRUCTURE;

ANIMALS; DIENCEPHALON; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; SONGBIRDS; SOUTH AMERICA; SPECIES SPECIFICITY; SUBSTANCE P; TELENCEPHALON;

EID: 33645957339     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.20915     Document Type: Article

References (96)

1. Aste N, Viglietti-Panzica C, Fasolo A, Panzica GC. 1995. Mapping of neurochemical markers in quail central nervous system: VIP- and SP-like immunoreactivity. J Chem Neuroanat 8:87-102.
2. Atoji Y, Wild JM. 2004. Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. J Comp Neurol 475:426-461.
3. Atoji Y, Wild JM, Yamamoto Y, Suzuki Y. 2002. Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447:177-199.
4. Benowitz LI, Karten HJ. 1976. The tractus infundibuli and other afferents to the parahippocampal region of the pigeon. Brain Res 102:174-180.
5. Berk ML, Hawkin RF. 1985. Ascending projections of the mammillary region in the pigeon: emphasis on telencephalic connections. J Comp Neurol 239:330-340.
6. Bingman VP. 1992. The importance of comparative studies and ecological validity for understanding hippocampal structure and cognitive function. Hippocampus 2:213-219.
7. Bingman VP, Ioale P, Casini G, Bagnoli P. 1990. The avian hippocampus: evidence for a role in the development of the homing pigeon navigational map. Behav Neurosci 104:906-911.
8. Bingman VP, Hough GE 2nd, Kahn MC, Siegel JJ. 2003. The homing pigeon hippocampus and space: in search of adaptive specialization. Brain Behav Evol 62:117-127.
9. Borhegyi Z, Leranth C. 1997a. Distinct substance P- and calretinin-containing projections from the supramammillary area to the hippocampus in rats: a species difference between rats and monkeys. Exp Brain Res 115:369-374.
10. Borhegyi Z, Leranth C. 1997b. Substance P innervation of the rat hippocampal formation. J Comp Neurol 384:41-58.
11. Bowden JJ, Garland AM, Baluk P, Lefevre P, Grady EF, Vigna SR, Bunnett NW, McDonald DM. 1994. Direct observation of substance P-induced internalization of neurokinin 1 (NK1) receptors at sites of inflammation. Proc Natl Acad Sci U S A 91:8964-8968.
12. Brenowitz EA. 1997. Comparative approaches to the avian song system. J Neurobiol 33:517-531.
13. 3H-proline. J Comp Neurol 245:454-470.
14. Casini G, Fontanesi G, Bingman VP, Jones TJ, Gagliardo A, Ioale P, Bagnoli P. 1997. The neuroethology of cognitive maps: contributions from research on the hippocampus and homing pigeon navigation. Arch Ital Biol 135:73-92.
15. Cavalieri B. 1635. Geometria indivisibilibus continuorum. Bononi: Typis Clemetis Feronij.
16. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497-3500.
17. Clayton NS. 1998. Memory and the hippocampus in food-storing birds: a comparative approach. Neuropharmacology 37:441-452.
18. Clayton NS, Reboreda JC, Kacelnik A. 1997. Seasonal changes of hippocampus volume in parasitic cowbirds. Behav Process 41:237-243.
19. Colombo M, Broadbent NJ, Taylor CS, Frost N. 2001. The role of the avian hippocampus in orientation in space and time. Brain Res 919:292-301.
20. Cuello AC, Galfre G, Milstein C. 1979. Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci U S A 76:3532-3536.
21. Davies NB. 2000. Cuckoos, cowbirds and other cheats: London: T & A. D. Poyser.
22. Del Fiacco M, Levanti MC, Dessi ML, Zucca G. 1987. The human hippocampal formation and parahippocampal gyms: localization of substance P-like immunoreactivity in newborn and adult post-mortem tissue. Neuroscience 21:141-150.
23. Dufty AM. 1982. Movements and activities of radio-tracked brown-headed cowbirds. Auk 99:316-327.
24. Ehrlich D, Keyser KT, Karten HJ. 1987. Distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). J Comp Neurol 266:220-233.
25. Erichsen JT, Reiner A, Karten HJ. 1982. Co-occurrence of substance P-like and Leu-enkephalin-like immunoreactivities in neurones and fibres of avian nervous system. Nature 295:407-410.
26. Erichsen JT, Bingman VP, Krebs JR. 1991. The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia): a basis for regional subdivisions. J Comp Neurol 314:478-492.
27. Fraga RM. 1988. Nest sites and breeding success of baywinged cowbirds Molothrus-Badius. J Ornithol 129:175-184.
28. Fraga R. 1998. Interactions of the parasitic screaming and shiny cowbirds (Molothrus rufoaxillaris and M. bonariensis) with a shared host, the bay-winged cowbird (M. badius). In: Rothstein SI, Robinson SK, editors. Parasitic birds and their hosts, studies in co-evolution. New York: Oxford University Press.
29. Freeman S, Zink Roberts M. 1995. A phylogenetic study of the blackbirds based on variation in mitochondrial DNA restriction sites. System Biol 44:409-420.
30. Friedmann H. 1929. The cowbirds, a study in the biology of the social parasitism. Springfield, IL: Charles C. Thomas.
31. Gagliardo A, Ioale P, Bingman VP. 1999. Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J Neurosci 19:311-315.
32. Gahr M. 1997. How should brain nuclei be delineated? Consequences for developmental mechanisms and for correlations of area size, neuron numbers and functions of brain nuclei. Trends Neurosci 20:58-62.
33. Gallagher AW, Chahl LA, Lynch AM. 1992. Distribution of substance P-like immunoreactivity in guinea pig central nervous system. Brain Res Bull 29:199-207.
34. Gould KL, Newman SW, Tricomi EM, DeVoogd TJ. 2001. The distribution of substance P and neuropeptide Y in four songbird species: a comparison of food-storing and non-storing birds. Brain Res 918:80-95.
35. Hampton RR, Shettleworth SJ. 1996. Hippocampus and memory in a food-storing and in a nonstoring bird species. Behav Neurosci 110:946-964.
36. Hasenohrl RU, Frisch C, Nikolaus S, Huston JP. 1994. Chronic administration of neurokinin SP improves maze performance in aged Rattus norvegicus. Behav Neural Biol 62:110-120.
37. Hökfelt T, Lundberg JM, Schultzberg M, Johansson O, Skirboll L, Anggard A, Fredholm B, Hamberger B, Pernow B, Rehfeld J, Goldstein M. 1980. Cellular localization of peptides in neural structures. Proc R Soc Lond B Biol Sci 210:63-77.
38. Hough GE 2nd, Pang KC, Bingman VP. 2002. Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation-evoked field potentials. J Comp Neurol 452:297-309.
39. Howard CV, Reed MG. 1998. Unbiased stereology. Oxford: Bios Scientific Publishers.
40. Hoy G, Ottow J. 1964. Biological and oological studies of the molothrine cowbirds (Icteridae) of Argentina. Auk 82:186-203.
41. Huston JP, Hasenohrl RU. 1995. The role of neuropeptides in learning: focus on the neurokinin substance P. Behav Brain Res 66:117-127.
42. Ino T, Itoh K, Sugimoto T, Kaneko T, Kamiya H, Mizuno N. 1988. The supramammillary region of the cat sends substance P-like immunoreactive axons to the hippocampal formation and the entorhinal cortex. Neurosci Lett 90:259-264.
43. Johnsgard PA. 1997. The avian brood parasites: deception at the nest. New York: Oxford University Press.
44. Johnson K, Lanyon S. 1999. Molecular systematics of the grackle and allies, and the effect of additional sequence (CYT B and ND2). Auk 116:759-768.
45. Kahn MC, Hough GE 2nd, Ten Eyck GR, Bingman VP. 2003. Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study. J Comp Neurol 459:127-141.
46. Krebs JR. 1990. Food-storing birds: adaptive specialization in brain and behaviour? Philos Trans R Soc Lond B Biol Sci 329:153-160.
47. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL. 1989. Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388-1392.
48. Krebs JR, Erichsen JT, Bingman VP. 1991. The distribution of neurotransmitters and neurotransmitter-related enzymes in the dorsomedial telencephalon of the pigeon (Columba livia). J Comp Neurol 314:467-477.
49. Lanyon SM. 1992. Interspecific brood parasitism in blackbirds icterinae a phylogenetic perspective. Science 255:77-79.
50. Leranth C, Nitsch R. 1994. Morphological evidence that hypothalamic substance P-containing afferents are capable of filtering the signal flow in the monkey hippocampal formation. J Neurosci 14:4079-4094.
51. Leranth C, Shanabrough M. 2001. Supramammillary area mediates subcortical estrogenic action on hippocampal synaptic plasticity. Exp Neurol 167:445-450.
52. Leranth C, Carpi D, Buzsaki G, Kiss J. 1999. The entorhino- septosupramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm. Neuroscience 88:701-718.
53. Lowther P. 2001. New name for the Bolivian blackbird. Bull Br Ornithol Club 121:280-281.
54. Mantyh PW, Allen CJ, Ghilardi JR, Rogers SD, Mantyh CR, Liu H, Basbaum AI, Vigna SR, Maggio JE. 1995. Rapid endocytosis of a G protein-coupled receptor: substance P-evoked internalization of its receptor in the rat striatum in vivo. Proc Natl Acad Sci U S A 92:2622-2626.
55. Mattioli R, Santangelo EM, Costa AC, Vasconcelos L. 1997. Substance P facilitates memory in goldfish in an appetitively motivated learning task. Behav Brain Res 85:117-120.
56. McNaughton N, Logan B, Panickar KS, Kirk IJ, Pan WX, Brown NT, Heenan A. 1995. Contribution of synapses in the medial supramammillary nucleus to the frequency of hippocampal theta rhythm in freely moving rats. Hippocampus 5:534-545.
57. Mermoz ME, Reboreda JC. 1999. Egg-laying behaviour by shiny cowbirds parasitizing brown-and-yellow marshbirds. Anim Behav 58:873-882.
58. Montagnese CM, Krebs JR, Szekely AD, Csillag A. 1993. A subpopulation of large calbindin-like immunopositive neurones is present in the hippocampal formation in food-storing but not in non-storing species of bird. Brain Res 614:291-300.
59. Montagnese CM, Krebs JR, Meyer G. 1996. The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tissue Res 283:263-282.
60. Nitsch R, Leranth C. 1994. Substance P-containing hypothalamic afferents to the monkey hippocampus: an immunocytochemical, tracing, and coexistence study. Exp Brain Res 101:231-240.
61. Nordeen KW, Nordeen EJ. 1997. Anatomical and synaptic substrates for avian song learning. J Neurobiol 33:532-548.
62. Nottebohm F. 1980. Brain pathways for vocal learning in birds: A review of the first 10 years. Prog Psychobiol Physiol Psychol 9:85-124.
63. Ortega CP. 1998. Cowbirds and other brood parasites: Tucson: The University of Arizona Press.
64. Otsuka M, Yoshioka K. 1993. Neurotransmitter functions of mammalian tachykinins. Physiol Rev 73:229-308.
65. Papadimitriou A, Wynne CD. 1999. Preserved negative patterning and impaired spatial learning in pigeons (Columba livia) with lesions of the hippocampus. Behav Neurosci 113:683-690.
66. Reboreda JC, Clayton NS, Kacelnik A. 1996. Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport 7(2):505-508.
67. Redies C, Puelles L. 2001. Modularity in vertebrate brain development and evolution. Bioessays 23:1100-1111.
68. Rehkamper G, Haase E, Frahm HD. 1988. Allometric comparison of brain weight and brain structure volumes in different breeds of the domestic pigeon, Columba livia f.d. (fantails, homing pigeons, strassers). Brain Behav Evol 31:141-149.
69. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Guturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
70. Rosenstock J, Field TD, Greene E. 1977. The role of mammillary bodies in spatial memory. Exp Neurol 55:340-352.
71. Rothstein SI, Verner J, Stevens E. 1984. Radio-tracking confirms a unique diurnal pattern of spatial occurrence in the parasitic brown-headed cowbird. Ecology 65:77-88.
72. Santangelo EM, Morato S, Mattioli R. 2001. Facilitatory effect of substance P on learning and memory in the inhibitory avoidance test for goldfish. Neurosci Lett 303:137-139.
73. Santin LJ, Rubio S, Begega A, Arias JL. 1999. Effects of mammillary body lesions on spatial reference and working memory tasks. Behav Brain Res 102:137-150.
74. Schlesinger K, Pelleymounter MA, van de Kamp J, Bader DL, Stewart JM, Chase TN. 1986. Substance P facilitation of memory: effects in an appetitively motivated learning task. Behav Neural Biol 45:230-239.
75. Sealy SG. 1992. Removal of yellow warbler eggs in association with cowbird parasitism. Condor 94:40-54.
76. Seress L, Leranth C. 1996. Distribution of substance P-immunoreactive neurons and fibers in the monkey hippocampal formation. Neuroscience 71:633-650.
77. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V. 2002. The tachykinin peptide family. Pharmacol Rev 54:285-322.
78. Sherry DF. 1997. Cross-species comparisons. Ciba Found Symp 208:181-189; discussion 189-194.
79. Sherry DF, Vaccarino AL. 1989. Hippocampus and memory for food caches in black-capped chickadees. Behav Neurosci 103:308-313.
80. Sherry DF, Vaccarino AL, Buckenham K, Herz RS. 1989. The hippocampal complex of food-storing birds. Brain Behav Evol 34:308-317.
81. Sherry DF, Forbes MRL, Khurgel M, Ivy GO. 1993. Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc Natl Acad Sci U S A 90:7839-7843.
82. Siegel JJ, Nitz D, Bingman VP. 2002. Electrophysiological profile of avian hippocampal unit activity: a basis for regional subdivisions. J Comp Neurol 445:256-268.
83. Strasser R, Bingman VP. 1999. The effects of hippocampal lesions in homing pigeons on a one-trial food association task. J Comp Physiol A185:583-590.
84. Szekely AD. 1999. The avian hippocampal formation: subdivisions and connectivity. Behav Brain Res 98:219-225.
85. Szekely AD, Krebs JR. 1996. Efferent connectivity of the hippocampal formation of the zebra finch (Taenopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin. J Comp Neurol 368:198-214.
86. Sziklas V, Petrides M. 1998. Memory and the region of the mammillary bodies. Prog Neurobiol 54:55-70.
87. Sziklas V, Petrides M. 2000. Selectivity of the spatial learning deficit after lesions of the mammillary region in rats. Hippocampus 10:325-328.
88. Thinschmidt JS, Kinney GG, Kocsis B. 1995. The supramammillary nucleus: is it necessary for the mediation of hippocampal theta rhythm? Neuroscience 67:301-312.
89. Tomaz C, Huston JP. 1986. Facilitation of conditioned inhibitory avoidance by post-trial peripheral injection of substance P. Pharmacol Biochem Behav 25:469-472.
90. Tomaz C, Nogueira PJ. 1997. Facilitation of memory by peripheral administration of substance P. Behav Brain Res 83:143-145.
91. Tombol T, Davies DC, Nemeth A, Sebesteny T, Alpar A. 2000. A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat Embryol 201:85-101.
92. Vann SD, Aggleton JP. 2004. The mammillary bodies: two memory systems in one? Nat Rev Neurosci 5:35-44.
93. Wetzel W, Matthies H. 1982. Effect of substance P on the retention of a brightness discrimination task in rats. Acta Biol Med Ger 41:647-652.
94. Wiley JW. 1988. Host selection by the shiny cowbird. Condor 90:289-303.
95. Yanagihara M, Niimi K. 1989. Substance P-like immunoreactive projection to the hippocampal formation from the posterior hypothalamus in the cat. Brain Res Bull 22:689-694.
96. Zupanc GK. 1996. Peptidergic transmission: from morphological correlates to functional implications. Micron 27:35-91.