Is the avian hippocampus a functional homologue of the mammalian hippocampus?

Neuroscience and Biobehavioral Reviews

Volumn 24, Issue 4, 2000, Pages 465-484

  Colombo, M ^a   Broadbent, N ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Area parahippocampalis; Avian; Concurrent discrimination; Hippocampus; Matching to sample; Pigeon; Spatial discrimination; Visual discrimination

Indexed keywords

ANIMAL EXPERIMENT; BIRD; BRAIN INJURY; HIPPOCAMPUS; MAMMAL; MONKEY; NONHUMAN; PIGEON; PRIORITY JOURNAL; RAT; REVIEW; SPATIAL DISCRIMINATION; VISUAL DISCRIMINATION;

ANIMALS; BEHAVIOR, ANIMAL; BIRDS; HIPPOCAMPUS; HUMANS; MAMMALS; SPECIES SPECIFICITY; VISUAL PERCEPTION;

EID: 0034105888     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(00)00016-6     Document Type: Review

References (176)

1. Gagliardo A., Ioale P., Bingman V.P. Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. Journal of Neuroscience. 19:1999;311-315.
2. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry. 20:1957;11-21.
3. Corkin S. Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H.M. Seminars in Neurology. 4:1984;249-259.
4. Gabrieli J.D.E., Cohen N.J., Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain and Cognition. 7:1988;157-177.
5. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clinical Neurosurgery. 19:1972;421-446.
6. Milner B., Corkin S., Teuber H.-L. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia. 6:1968;215-234.
7. Cummings J.L., Tomiyasu U., Read S., Benson D.F. Amnesia with hippocampal lesions after cardiopulmonary arrest. Neurology. 34:1984;679-681.
8. Victor M., Agamanolis D. Amnesia due to lesions confined to the hippocampus: a clinical-pathologic study. Journal of Cognitive Neuroscience. 2:1990;246-257.
9. Victor M., Angevine J.B., Mancall E.L., Fisher C.M. Memory loss with lesions of the hippocampal formation. Archives of Neurology. 5:1961;244-263.
10. Cave C.B., Squire L.R. Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus. 2:1992;151-164.
11. Smith M.L., Milner B. The role of the right hippocampus in the recall of spatial locationl. Neuropsychologia. 19:1981;781-793.
12. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Review. 99:1992;195-231.
13. Angeli S.J., Murray E.A., Mishkin M. Hippocampectomized monkeys can remember one place but not two. Neuropsychologia. 31:1993;1021-1030.
14. Aggleton J.P., Blindt H.S., Rawlins J.N.P. Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats. Behavioral Neuroscience. 103:1989;962-974.
15. Aggleton J.P., Hunt P.R., Rawlins J.N.P. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behavioural Brain Research. 19:1986;133-146.
16. Mishkin M. Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature. 273:1978;297-298.
17. Mishkin M. A memory system in the monkey. Philosophical Transactions of the Royal Society of London. 298B:1982;85-92.
18. Morris R.G.M., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 297:1982;681-683.
19. Olton D.S., Becker J.T., Handelmann G.E. Hippocampus, space, and memory. Behavioral and Brain Sciences. 2:1979;313-365.
20. Parkinson J.K., Murray E.A., Mishkin M. A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. Journal of Neuroscience. 8:1988;4159-4167.
21. Raffaele K.C., Olton D.S. Hippocampal and amygdaloid involvement in working memory for nonspatial stimuli. Behavioral Neuroscience. 102:1988;349-355.
22. Zola-Morgan S., Squire L.R. Memory impairment in monkeys following lesions limited to the hippocampus. Behavioral Neuroscience. 100:1986;155-160.
23. O'Keefe J., Nadel L. The hippocampus as a cognitive map. 1978;Oxford University Press, Oxford.
24. Eichenbaum H., Otto T., Cohen N.J. Two functional components of the hippocampal memory system. Behavioral and Brain Sciences. 17:1994;449-518.
25. Szabo J., Cowan W.M. A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). Journal of Comparative Neurology. 222:1984;265-300.
26. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1998;Academic Press, San Diego.
27. Karten H.J., Hodos W.A. Stereotaxic atlas of the brain of the pigeon (Columba livia). 1967;The Johns Hopkins Press, Baltimore.
28. Bingman V.P. Vision, cognition, and the avian hippocampus. Zeigler H.P., Bischof H.-J. Vision, brain, and behavior in birds. 1993;391-408 MIT Press, Cambridge, MA.
29. Casini G., Bingman V.P., Bagnoli P. Connections of the pigeon dorsomedial forebrain studied with WGA-HRP and 3H-Proline. Journal of Comparative Neurology. 245:1986;454-470.
30. Krayniak P.F., Siegel A. Efferent connections of the hippocampus and adjacent regions in the pigeon. Brain Behaviour and Evolution. 15:1978;372-388.
31. Krebs J.R., Erichsen J.T., Bingman V.P. The distribution of neurotransmitters and neurotransmitter-related enzymes in the dorsomedial telencephalon of the pigeon (Columba livia). Journal of Comparative Neurology. 314:1991;467-477.
32. Erichsen J.T., Bingman V.P., Krebs J.R. The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia): a basis for regional subdivisions. Journal of Comparative Neurology. 314:1991;478-492.
33. Montagnese C.M., Krebs J.R., Meyer G. The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tissue Research. 283:1996;263-282.
34. Benowitz L.I., Karten H.J. The tractus infundibuli and other afferents to the parahippocampal region of the pigeon. Brain Research. 102:1976;174-180.
35. Bingman V.P., Bagnoli P., Ioale P., Casini G. Behavioral and anatomical studies of the avian hippocampus. Chan-Palay V., Kohler C. The hippocampus, new vistas. 1989;379-394 Liss, New York.
36. Craigie E.H. The hippocampal and parahippocampal cortex of the Emu (Dromiceius). Journal of Comparative Neurology. 61:1935;563-591.
37. Kallen B. Embryogenesis of brain nuclei in the chick telencephalon. Ergebnisse der Anatomie und Entwicklungsgeschichte. 36:1962;62-82.
38. Kuhlenbeck H. The ontogenetic development and phylogenetic significance of the cortex telencephali in the chick. Journal of Comparative Neurology. 69:1938;273-301.
39. Trottier C., Reperant J., Miceli D. Anatomical evidence of a retino-thalamo-hippocampal pathway in the pigeon (Columba livia). Journal of Brain Research. 36:1995;489-500.
40. Bons N., Bouille C., Bayle J.D., Assenmacher I. Light and electron microscopic evidence of hypothalamic afferences originating from the hippocampus in the pigeon. Experientia. 32:1976;1443-1445.
41. Bouille C., Raymond J., Bayle J.D. Retrograde transport of horseradish peroxidase from the nucleus posterior medialis hypothalami to the hippocampus and the medial septum in the pigeon. Neuroscience. 2:1977;435-439.
42. Molla R., Rodriguez J., Calvet S., Garcia-Verdugo J.M. Neuronal types of the cerebral cortex of the adult chicken, (Gallus gallus). A golgi study. Journal of Hirnforschung. 27:1986;381-390.
43. Margrie T.W., Rostas J.A.P., Sah P. Long-term potentiation of synaptic transmission in the avian hippocampus. Journal of Neuroscience. 18:1998;1207-1216.
44. Wieraszko A., Ball G.F. Long-term potentiation in the avian hippocampus does not require activation of the N-Methyl-D-Aspartate (NMDA) receptor. Synapse. 13:1993;173-178.
45. Colombo M., D'Amato M.R. A comparison of visual and auditory short-term memory in monkeys (Cebus apella). Quarterly Journal of Experimental Psychology, 38B. 1986;425-448.
46. Squire L.R., Zola-Morgan S. Memory: brain systems and behavior. Trends in Neurosciences. 11:1988;170-175.
47. Zola-Morgan S., Squire L.R., Amaral D.G., Suzuki W.A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience. 9:1989;4355-4370.
48. Zola-Morgan S., Squire L.R., Clower R.P., Rempel N.L. Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. Journal of Neuroscience. 13:1993;251-265.
49. Alvarez P., Zola-Morgan S., Squire L.R. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. Journal of Neuroscience. 15:1995;3796-3807.
50. Colombo M., Swain N., Harper D., Alsop B. The effects of hippocampal and area parahippocampalis lesions in pigeons. I. Delayed matching to sample. Quarterly Journal of Experimental Psychology, 50B. 1997;149-171.
51. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. Journal of Neuroscience. 6:1986;2950-2967.
52. Murray E.A. What have ablation studies told us about the neural substrates of stimulus memory? Seminars in the Neurosciences. 8:1996;13-22.
53. Murray E.A., Mishkin M. Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. Journal of Neuroscience. 6:1986;1991-2003.
54. Gaffan D., Murray E.A. Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. Behavioral Neuroscience. 106:1992;30-38.
55. Meunier M., Bachevalier J., Mishkin M., Murray E.A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. Journal of Neuroscience. 13:1993;5418-5432.
56. O'Boyle V.J. Jr, Murray E.A., Mishkin M. Effects of excitotoxic amygdalo-hippocampal lesions on visual recognition in rhesus monkeys. Society for Neuroscience Abstracts. 19:1995;438.
57. Suzuki W.A., Zola-Morgan S., Squire L.R., Amaral D.G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. Journal of Neuroscience. 13:1993;2430-2451.
58. Zola-Morgan S., Squire L.R., Amaral D.G. Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation. Journal of Neuroscience. 9:1989;1922-1936.
59. Zola-Morgan S., Squire L.R., Rempel N.L., Clower R.P., Amaral D.G. Enduring memory impairment in monkeys after ischemic damage to the hippocampus. Journal of Neuroscience. 12:1992;2582-2596.
60. Nadel L. Multiple memory systems: what and why. Journal of Cognitive Neuroscience. 4:1992;179-188.
61. Nadel L. Multiple memory systems: what and why, an update. Schacter D.L., Tulving E. Memory systems 1994. 1994;39-63 MIT Press, Cambridge, MA.
62. Teng E., Squire L.R., Zola S.M. Effects of removal from the testing apparatus on delayed nonmatching to sample performance in monkeys with lesions of the hippocampal region. Society for Neuroscience Abstracts. 24:1998;17.
63. Murray E.A., Mishkin M. Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. Journal of Neuroscience. 18:1998;6568-6582.
64. Mumby D.G., Wood E.R., Pinel J.P.J. Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala. Psychobiology. 20:1992;18-27.
65. Mumby D.G., Pinel J.P.J. Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience. 108:1994;11-18.
66. Sahgal A. Hippocampal lesions disrupt recognition memory in pigeons. Behavioural Brain Research. 11:1984;47-58.
67. Good M., Macphail E.M. The avian hippocampus and short-term memory for spatial and non-spatial information. Quarterly Journal of Experimental Psychology. 47B:1994;293-317.
68. Hampton R.R., Shettleworth S.J. Hippocampal lesions impair memory for location but not color in passerine birds. Behavioral Neuroscience. 110:1996;831-835.
69. Rawlins J.N.P., Lyford G.L., Seferiades A., Deacon R.M.J., Cassaday H.J. Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. Behavioral Neuroscience. 107:1993;420-433.
70. Rothblat L.A., Kromer L.F. Object recognition memory in the rat: the role of the hippocampus. Behavioural Brain Research. 42:1991;25-32.
71. Wan R-Q., Pang K., Olton D.S. Hippocampal and amygdaloid involvement in nonspatial and spatial working memory in rats: effects of delay and interference. Behavioral Neuroscience. 108:1994;866-882.
72. Milner B. Memory and the medial temporal regions of the brain. Pribram K.H., Broadbent D.E. Biology of memory. 1970;29-50 Academic Press, New York.
73. Mahut H., Zola-Morgan S., Moss M. Hippocampal resections impair associative learning and recognition memory in the monkey. Journal of Neuroscience. 2:1982;1214-1229.
74. Zola-Morgan S., Squire L.R. Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behavioral Neuroscience. 99:1985;22-34.
75. Jarrard L.E. Role of interference in retention by rats with hippocampal lesions. Journal of Comparative and Physiological Psychology. 89:1975;400-408.
76. D'Amato M.R. Delayed matching and short-term memory in monkeys. Bower G.H. The psychology of learning and motivation. Advances in theory and research. 7:1973;227-269 Academic Press, New York.
77. Kojima S. Auditory short-term memory in the japanese monkey. International Journal of Neuroscience. 25:1985;255-262.
78. Grant D.S. Proactive interference in pigeon short-term memory. Journal of Experimental Psychology: Animal Behavior Processes. 1:1975;207-220.
79. Holt G.L., Shafer J.N. Function of intertrial interval in matching-to-sample. Journal of the Experimental Analysis of Behavior. 19:1973;181-186.
80. Roberts W.A., Kraemer P.J. Some observations of the effects of intertrial interval and delay on delayed matching to sample in pigeons. Journal of Experimental Psychology: Animal Behavior Processes. 8:1982;342-353.
81. Sidman M., Stoddard L.T., Mohr J.P. Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions. Neuropsychologia. 6:1968;245-254.
82. Colombo M., Graziano M. Effects of auditory and visual interference on auditory-visual delayed matching-to-sample in monkeys (Macaca fascicularis). Behavioral Neuroscience. 108:1994;636-639.
83. Etkin M.W. Light produced interference in a delayed matching task with capuchin monkeys. Learning and Motivation. 3:1972;313-324.
84. Grant D.S., Roberts W.A. Sources of retroactive inhibition in pigeon short-term memory. Journal of Experimental Psychology: Animal Behavior Processes. 2:1976;1-16.
85. Maki W.S., Moe J.C., Bierley C.M. Short-term memory for stimuli, responses, and reinforcers. Journal of Experimental Psychology: Animal Behavior Processes. 3:1977;156-177.
86. Aggleton J.P., Kentridge R.W., Sembi S. Lesions of the fornix but not the amygdala impair the acquisition of concurrent discriminations by rats. Behavioural Brain Research. 48:1991;103-112.
87. Aggleton J.P., Shaw C., Gaffan E.A. The performance of postencephalitic amnesic subjects on two behavioral tests of memory: concurrent discrimination learning and delayed matching-to-sample. Cortex. 28:1992;359-372.
88. Correll R.E., Scoville W.B. Effects of medial temporal lesions on visual discrimination performance. Journal of Comparative and Physiological Psychology. 60:1965;175-181.
89. Correll R.E., Scoville W.B. Relationship of iti to acquisition of serial visual discriminations following temporal rhinencephalon resection in monkeys. Journal of Comparative and Physiological Psychology. 70:1970;464-469.
90. George P.J., Horel J.A., Cirillo R.A. Reversible cold lesions of the parahippocampal gyrus in monkeys result in deficits on the delayed match-to-sample and other visual tasks. Behavioural Brain Research. 34:1989;163-178.
91. Moss M., Mahut H., Zola-Morgan S. Concurrent discrimination learning of monkeys after hippocampal, entorhinal, or fornix lesions. Journal of Neuroscience. 1:1981;227-240.
92. Oscar-Berman M., Zola-Morgan S.M. Comparative neuropsychology and Korsakoff's syndrome. II. Two-choice visual discrimination learning. Neuropsychologia. 18:1980;513-525.
93. Squire L.R., Zola-Morgan S., Chen K.S. Human amnesia and animal models of amnesia: performance of amnesic patients on tests designed for the monkey. Behavioral Neuroscience. 11:1988;210-221.
94. Wible C.G., Shiber J.R., Olton D.S. Hippocampus, fimbria-fornix, amygdala, and memory: object discrimination in rats. Behavioral Neuroscience. 106:1992;751-761.
95. Colombo M., Cawley S., Broadbent N. The effects of hippocampal and area parahippocampalis lesions in pigeons. II. Concurrent discrimination and spatial memory. Quarterly Journal of Experimental Psychology, 50B. 1997;172-189.
96. Buckley M.J., Gaffan D. Impairments of visual object-discrimination learning after perirhinal cortex ablation. Behavioral Neuroscience. 111:1997;467-475.
97. Buffalo E.A., Steffanacci L., Squire L.R., Zola S.M. A reexamination of the concurrent discrimination learning task: the importance of anterior inferotemporal cortex, area TE. Behavioral Neuroscience. 112:1998;3-14.
98. Aggleton J.P., Nicol R.M., Huston A.E., Fairbairn A.F. The performance of amnesic subjects on tests of experimental amnesia in animals: delayed matching-to-sample and concurrent learning. Neuropsychologia. 26:1988;265-272.
99. Mumby D.G., Pinel J.P.J., Kornecook T.J., Shen M.J., Redila V.A. Memory deficits following lesions of hippocampus or amygdala in rat: assessment by an object-memory test battery. Psychobiology. 23:1995;26-36.
100. Deacon R.M.J., Rawlins J.N.P. Effects of aspiration lesions of hippocampus or overlying neocortex on concurrent and configural object discriminations in rats. Behavioral Brain Research. 77:1996;165-174.
101. Jarrard L.E. On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. Journal of Neuroscience Methods. 29:1989;251-259.
102. Jarrard L.E., Davidson T.L. On the hippocampus and learned conditional responding: effects of aspiration versus ibotenate lesions. Hippocampus. 1:1991;107-117.
103. Rothblat L.A., Vnek N., Gleason T.C., Kromer L.F. Role of the parahippocampal region in spatial and nonspatial memory: effects of parahippocampal lesions on rewarded alternation and concurrent object discrimination learning in the rat. Behavioural Brain Research. 55:1993;93-100.
104. Broadbent N., Colombo M. Visual discrimination and negative patterninig performance following bilateral ablation to the pigeon hippocampus and area parahippocampalis. Society for Neuroscience: Abstracts. 23:1997;2127.
105. Rudy J.W., Sutherland R.J. The hippocampal formation is necessary for rats to learn and remember configural discriminations. Behavioural Brain Research. 34:1989;97-109.
106. Rudy J.W., Sutherland R.J. Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus. 5:1995;375-389.
107. Sutherland R.J., Rudy J.W. Configural association theory: the role of the hippocampal formation in learning, memory, and amnesia. Psychobiology. 17:1989;129-144.
108. Alvarado M.C., Rudy J.W. A comparison of kainic acid plus colchicine and ibotenic acid-induced hippocampal formation damage on four configural tasks in rats. Behavioral Neuroscience. 109:1995;1052-1062.
109. Sutherland R.J., McDonald R.J. Hippocampus, amygdala, and memory deficits in rats. Behavioural Brain Research. 37:1990;57-79.
110. Davidson T.L., McKernan M.G., Jarrard L.E. Hippocampal lesions do not impair negative patterning: a challenge to configural association theory. Behavioral Neuroscience. 107:1993;227-234.
111. Skinner D.M., Van Der Kooy D. Acquisition and retention of negative patterning in hippocampal-lesioned rats. Psychobiology. 25:1997;10-17.
112. Broadbent N., Gallagher S., Colombo M. Hippocampal lesions and negative patterning in pigeons. Psychobiology. 27:1999;51-56.
113. McDonald R.J., Murphy R.A., Guarraci F.A., Gortler J.R., White N.M., Baker A.G. Systematic comparison of the effects of hippocampal and fimbria-fornix lesions on acquisition of three configural discriminations. Hippocampus. 7:1997;371-388.
114. Han J.S., Gallagher M., Holland P. Hippocampal lesions enhance configural learning by reducing proactive interference. Hippocampus. 8:1998;138-146.
115. Gallistel C.R. The organization of learning. 1990;MIT Press, Cambridge, MA.
116. Maguire E.A. Hippocampal involvement in human topographical memory: evidence from functional imaging. Philosophical Transactions of the Royal Society of London. 352B:1997;1475-1480.
117. Maguire E.A., Frackowiak R.S.J., Frith C.D. Learning to find your way: a role for the human hippocampal formation. Proceedings of the Royal Society of London. 263B:1996;1745-1750.
118. Maguire E.A., Frackowiak R.S.J., Frith C.D. Recalling routes around London: activation of the right hippocampus in taxi drivers. Journal of Neuroscience. 17:1997;7103-7110.
119. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S.J., Frith C.D., O'Keefe J. Knowing where and getting there: a human navigation network. Science. 280:1998;921-924.
120. Olton D.S., Collison C., Werz M.A. Spatial memory and radial arm maze performance of rats. Learning and Motivation. 8:1977;289-314.
121. Olton D.S., Samuelson R.J. Remembrance of places passed: spatial memory in rats. Journal of Experimental Psychology: Animal Behavior Processes. 2:1976;97-115.
122. Olton D.S. Spatial memory. Scientific American. 236:1977;82-98.
123. Morris R.G.M. Spatial localisation does not require the presence of local cues. Learning and Motivation. 12:1981;239-260.
124. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods. 11:1984;47-60.
125. Sutherland R.J., Kolb B., Whishaw I.Q. Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neuroscience Letters. 31:1982;271-276.
126. Sutherland R.J., Whishaw I.Q., Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behavioral Brain Research. 7:1983;133-153.
127. Papi F., Wallraff H. Avian navigation. 1982;Springer, Berlin.
128. Bingman V.P., Ioale P., Casini G., Bagnoli P. The avian hippocampus: evidence for a role in the development of the homing pigeon navigational map. Behavioral Neuroscience. 104:1990;906-911.
129. Papi F., Casini G. Pigeons with ablated pyriform cortex home from familiar but not from unfamiliar sites. Proceedings of the National Academy of Sciences USA. 87:1990;3783-3787.
130. Bingman V.P., Bagnoli P., Ioale P., Casini G. Homing behaviour of pigeons after telencephalic ablations. Brain Behaviour and Evolution. 24:1984;94-108.
131. Bingman V.P., Ioale P., Casini G., Bagnoli P. Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons. Behavioural Brain Research. 27:1988;179-187.
132. Bingman V.P., Yates G. Hippocampal lesions impair navigational learning in experienced homing pigeons. Behavioral Neuroscience. 106:1992;229-232.
133. Bingman V.P., Mench J.A. Homing behaviour of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behavioural Brain Research. 40:1990;227-238.
134. Fremouw T., Jackson-Smith P., Kesner R.P. Impaired place learning and unimpaired cue learning in hippocampal-lesioned pigeons. Behavioral Neuroscience. 111:1997;963-975.
135. Pearce J.M., Roberts A.D.L., Good M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature. 396:1998;75-77.
136. Cave C.B., Squire L.R. Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus. Hippocampus. 3:1991;329-340.
137. Smith M.L. Recall of spatial location by the amnesic patient H.M. Brain and Cognition. 7:1988;178-183.
138. Smith M.L., Milner B. Right hippocampal impairment in the recall of spatial location: encoding deficits or rapid forgetting. Neuropsychologia. 27:1989;71-81.
139. Milner B. Visually-guided maze learning in man: effects of bilateral hippocampal, bilateral frontal, and unilateral cerebral lesions. Neuropsychologia. 3:1965;317-338.
140. Feigenbaum J.D., Polkey C.E., Morris R.G. Deficits in spatial working memory after unilateral temporal lobectomy in man. Neuropsychologia. 34:1996;163-176.
141. Olton D.S., Papas B.C. Spatial memory and hippocampal function. Neuropsychologia. 17:1979;669-682.
142. Good M. The effects of hippocampal-area parahippocampalis lesions on discrimination learning in the pigeon. Behavioural Brain Research. 26:1987;171-184.
143. Bond A.B., Cook R.G., Lamb M.R. Spatial memory and the performance of rats and pigeons in the radial-arm maze. Animal Learning & Behavior. 9:1981;575-580.
144. Olson D.J., Maki W.S. Characteristics of spatial memory in pigeons. Journal of Experimental Psychology: Animal Behavior Processes. 9:1983;266-280.
145. Roberts W.A., Van Veldhuizen N. Spatial memory in pigeons on the radial maze. Journal of Experimental Psychology: Animal Behavior Processes. 11:1985;241-260.
146. Spetch M.L., Edwards C.A. Spatial memory in pigeons (Columba livia) in an open-field feeding environment. Journal of Comparative Psychology. 100:1986;266-278.
147. Spetch M.L., Honig W.K. Characteristics of pigeons' spatial working memory in an open-field task. Animal Learning & Behavior. 16:1988;123-131.
148. Harrell L.E., Barlow T.S., Parsons D. Cholinergic neurons, learning, and recovery of function. Behavioral Neuroscience. 101:1987;644-652.
149. Janis L.S., Bishop T.W., Dunbar G.L. Medial septal lesions in rats produce permanent deficits for strategy selection in a spatial memory task. Behavioral Neuroscience. 108:1994;892-898.
150. Brown P.L., Jenkins H.M. Auto-shaping of the pigeon's key-peck. Journal of the Experimental Analysis of Behavior. 11:1968;1-8.
151. Williams D.R., Williams H. Auto-maintenance in the pigeon: sustained pecking despite contingent non-reinforcement. Journal of the Experimental Analysis of Behavior. 12:1969;511-520.
152. Reilly S., Good M. Hippocampal lesions and associative learning in the pigeon. Behavioral Neuroscience. 103:1989;731-742.
153. Good M., Honey R.C. Conditioning and contextual retrieval in hippocampal rats. Behavioral Neuroscience. 105:1991;499-509.
154. Good M., Macphail E.M. Hippocampal lesions in pigeons (Columba livia) disrupt reinforced preexposure but not overshadowing or blocking. Quarterly Journal of Experimental Psychology. 47B:1994;263-291.
155. Colombo M., Broadbent N.J. A comparison of the effects of hippocampal lesions in pigeons and monkeys: evidence for a functional homology. Society for Neuroscience Abstracts. 25:1999;2160.
156. Hirsh R. The hippocampus and contextual retrieval of information from memory: a theory. Behavioral Biology. 12:1974;421-444.
157. Hirsh R. The hippocampus, conditional operations, and cognition. Physiological Psychology. 8:1980;175-182.
158. Honey R.C., Willis A., Hall G. Context specificity in pigeon autoshaping. Learning and Motivation. 21:1990;125-136.
159. Gray J.A. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. 1982;Oxford University Press, Oxford.
160. Gray J.A., McNaughton N. Comparison between the behavioural effects of septal and hippocampal lesions: a review. Neuroscience & Biobehavioral Reviews. 7:1983;119-188.
161. Douglas R.J. The hippocampus and behavior. Psychological Bulletin. 67:1967;416-442.
162. Kimble D.P. Hippocampus and internal inhibition. Psychological Bulletin. 70:1968;285-295.
163. Kimble D.P., Kimble R.J. Hippocampectomy and response perseveration in the rat. Journal of Comparative and Physiological Psychology. 3:1965;474-476.
164. Blanchard R.J., Fial R.A. Effects of limbic lesions on passive avoidance and reactivity to shock. Journal of Comparative and Physiological Psychology. 66:1968;600-612.
165. Kimble D.P. The effects of bilateral hippocampal lesions in rats. Journal of Comparative and Physiological Psychology. 56:1963;273-283.
166. Jarrard L.E., Isaacson R.L., Wickelgren W.O. Effects of hippocampal ablation and intertrial interval on runway acquisition and extinction. Journal of Comparative and Physiological Psychology. 57:1964;442-444.
167. Good M., Honey R.C. Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behavioral Neuroscience. 111:1997;487-493.
168. Kaplan J. Approach and inhibitory reactions in rats after bilateral hippocampal damage. Journal of Comparative and Physiological Psychology. 65:1968;274-281.
169. Raphelson A.C., Isaacson R.L., Douglas R.J. The effects of distracting stimuli on the runway performance of limbic damaged rats. Psychonomic Science. 3:1965;483-484.
170. Wickelgren W.O., Isaacson R.L. Effect of the introduction of an irrelevant stimulus on runway performance of the hippocampectomized rat. Nature. 200:1963;48-50.
171. Dietrich A., Allen J.D., Bunnell B.N. Is the hippocampus involved in temporal discrimination and the memory of short intervals? International Journal of Neuroscience. 90:1997;255-270.
172. Bingman V.P., Strasser R., Baker C., Ritters L.V. Paired-associate learning is unaffected by combined hippocampal and parahippocampal lesions in homing pigeons. Behavioral Neuroscience. 112:1998;533-540.
173. Bunsey M., Eichenbaum H. Paired associate learning in rats: critical involvement of the parahippocampal region. Behavioral Neuroscience. 107:1993;740-747.
174. Bunsey M., Eichenbaum H. Selective hippocampal lesions facilitate performance in a paired associate task in rats. Society for Neuroscience Abstracts. 19:1993;358.
175. Cassaday H.J., Rawlins J.N.P. Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. Behavioral Neuroscience. 109:1995;594-606.
176. Cassaday H.J., Rawlins J.N.P. The hippocampus, objects, and their contexts. Behavioral Neuroscience. 111:1997;1228-1244.