The relative size of the avian hippocampus (Hp) has been shown to be related to spatial memory and food storing in two avian families, the parids and corvids. Basil et al. [Brain Behav Evol 1996;47:156–164] examined North American food-storing birds in the corvid family and found that Clark’s nutcrackers had a larger relative Hp than pinyon jays and Western scrub jays. These results correlated with the nutcracker’s better performance on most spatial memory tasks and their strong reliance on stored food in the wild. However, Pravosudov and de Kort [Brain Behav Evol 2006;67:1–9] raised questions about the methodology used in the 1996 study, specifically the use of paraffin as an embedding material and recalculation for shrinkage. Therefore, we measured relative Hp volume using gelatin as the embedding material in four North American species of food-storing corvids (Clark’s nutcrackers, pinyon jays, Western scrub jays and blue jays) and one Eurasian corvid that stores little to no food (azure-winged magpies). Although there was a significant overall effect of species on relative Hp volume among the five species, subsequent tests found only one pairwise difference, blue jays having a larger Hp than the azure-winged magpies. We also examined the relative size of the septum in the five species. Although Shiflett et al. [J Neurobiol 2002;51:215–222] found a difference in relative septum volume amongst three species of parids that correlated with storing food, we did not find significant differences amongst the five species in relative septum. Finally, we calculated the number of neurons in the Hp relative to body mass in the five species and found statistically significant differences, some of which are in accord with the adaptive specialization hypothesis and some are not.

Keywords:
Corvids, Food storing, Hippocampus, Septum, Telencephalon
1.
Balda RP (1980): Are seed-caching systems co-evolved; in Nohring R (ed): Acta XVII. Congressus Internationalis Ornithologici. Berlin, Deutsche Ornithologen-Gesellschaft, pp 1185–1191.
2.
Balda RP (1987): Avian impacts on pinyon-uniper woodlands; in Everett RL (ed): Proceedings: Pinyon-Juniper Conference, Reno NV January 13–16, 1986 (General Technical Report No. INT-215, pp. 525–533). Ogden, US Department of Agriculture, Forest Service, Intermountain Research Station.
3.
Balda RP, Kamil AC (1989): A comparative study of cache recovery by three corvid species. Anim Behav 38:486–495.
4.
Basil JA, Kamil AC, Balda RP, Fite KV (1996): Differences in hippocampal volume among food storing corvids. Brain Behav Evol 47:156–164.
5.
Bingman VP, Gagliardo A, Hough GE II, Ioale P, Kahn MC, Siegel JJ (2005): The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr Comp Biol 45:555–564.
6.
Brodin A, Lundborg K (2003): Is hippocampal volume affected by specialization for food hoarding in birds? Proc R Soc Lond B Biol Sci 270:1555–1563.
7.
Canario F, Boieiroa ND, Vicente L (2002): The nestling diet of the Iberian azure-winged magpie Cyanopica cyanus cooki in southeastern Portugal. Ardeola 49:283–286.
8.
Casini G, Bingman VP, Bagnoli P (1986): Connections of the pigeon dorsomedial forebrain studies with WGA-HRP and 3H-proline. J Comp Neurol 245:454–470.
9.
Chrobak JJ, Napier TC (1992): Antagonism of GABAergic transmission within the septum distrupts working/episodic memory in the rat. Neuroscience 47:833–841.
10.
Chrobak JJ, Stackman RR, Walsh TJ (1989): Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat. Behav Neural Biol 52:357–369.
11.
Clayton NS, Dickinson A (1998): Episodic-like memory during cache recovery by scrub jays. Nature 395:272–274.
12.
Clayton NS, Krebs JR (1994): Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 174:371–379.
13.
Cohen J (1988): Statistical Power Analysis for the Behavioral Sciences, ed 2. Hillsdale, Erlbaum.
14.
Colombo M, Broadbent N (2000): Is the avian hippocampus a functional homologue of the mammalian hippocampus. Neurosci Biobehav Rev 24:465–484.
15.
Curry RL, Peterson AT, Langen TA (2002): Western scrub-jay (Aphelocoma californica) ; in Poole A, Gill F (eds): The Birds of North America, No. 712. Philadelphia, Birds of North America.
16.
Darley-Hill S, Johnson WC (1981): Acorn dispersal by blue jays (Cyanocittae ristata). Oecologia 50:231–232.
17.
Eichenbaum H (2006): Memory binding in hippocampal relational networks; in Zimmer HD, Mecklinger A, Lindenberger U (eds): Handbook of Binding and Memory: Perspectives from Cognitive Neuroscience. Oxford, Oxford University Press, pp 25–51.
18.
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.
19.
Ericson PGP, Jansén A-L, Johansson US, Ekman J (2005): Inter-generic relationships of the crows, jays, magpies and allied groups (Aves: Corvidae) based on nucleotide sequence data. J Avian Biol 36:222–234.
20.
Garamszegi LZ, Eens M (2004): The evolution of hippocampus volume and brain size in relation to food hoarding in birds. Ecol Lett 7:1216–1224.
21.
Garamszegi LZ, Lucas JR (2005): Continental variation in relative hippocampal volume in birds: the phylogenetic extent of the effect and the potential role of winter temperatures. Biol Lett 1:330–333.
22.
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.
23.
Gould-Beierle KL (2000): A comparison of four corvid species in a working and reference memory task using a radial maze. J Comp Psychol 114:347–356.
24.
Hampton RR, Sherry DF, Shettleworth SJ, Khurgel M, Ivy G (1995): Hippocampal volume and food-storing behavior are related in parids. Brain Behav Evol 45:54–61.
25.
Hampton RR, Shettleworth SJ (1996): Hippocampus and memory in a food-storing and in a nonstoring bird species. Behav Neurosci 110:946–964.
26.
Healy SD (1995): Memory for objects and positions – delayed non-matching-to-sample in storing and nonstoring tits. QJ Exp Psychol B 48:179–191.
27.
Healy SD, Clayton NS, Krebs JR (1994): Development of hippocampus specialization in two species of tit (Parus spp.). Behav Brain Res 61:23–28.
28.
Healy SD, Krebs JR (1992): Food storing and the hippocampus in corvids: amount and volume are correlated. Proc R Soc Lond B 248:241–245.
29.
Healy SD, Krebs JR (1996): Food storing and the hippocampus in Paridae. Brain Behav Evol 47:195–199.
30.
Healy SD, Suhonen J (1996): Memory for locations of stored food in willow tits and marsh tits. Behaviour 133:71–80.
31.
Hope S (1989): Phylogeny of the Avian Family Corvidae; PhD dissertation, City University of New York, New York.
32.
Hoshooley JS, Sherry DF (2004): Neuron production, neuron number, and structure size are seasonally stable in the hippocampus of the food-storing black-capped chickadee (Poecile atricapillus). Behav Neurosci 118:345–355.
33.
Jacobs LF (2006): From movement to transitivity: The role of hippocampal parallel maps in configural learning. Rev Neurosci 17:99–109.
34.
Jarvis ED, Güntürkün O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB (2005): Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151–159.
35.
Johnson WC, Adkisson CS (1985): Dispersal of beech nuts by blue jays in fragmented landscapes. Am Midl Nat 113:319–324.
36.
Kamil AC, Balda RP (1985): Cache recovery and spatial memory in Clark’s nutcrackers (Nucifraga columbiana). J Exp Psychol Anim Behav Process 11:95–111.
37.
Kamil AC, Balda RP, Olson DJ (1994): Performance of four seed-caching corvid species in the radial-arm maze analog. J Comp Psychol 108:385–393.
38.
Karten HJ, Hodos W (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, Johns Hopkins.
39.
Krayniak PF, Siegel A (1978a): Efferent connections of the hippocampus and adjacent regions in the pigeon. Brain Behav Evol 15:372–388.
40.
Krayniak PF, Siegel A (1978b): Efferent connections of the septal area in the pigeon. Brain Behav Evol 15:389–404.
41.
Krebs JR (1990): Food-storing birds: adaptive specialization in brain and behavior? Phil Trans R Soc (Lond) B 329:55–62.
42.
Krebs JR, Clayton NS, Healy SD, Cristol DA, Patel SN, Jolliffe AR (1996): The ecology of the avian brain: food-storing memory and the hippocampus. Ibis 138:34–46.
43.
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.
44.
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.
45.
LaDage LD, Roth TC II, Fox RA, Pravosudov VV (2009): Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. Behav Neurosci 123:284–291.
46.
Ligon JD (1978): Reproductive interdependence of pinyon jays and pinyon pines. Ecol Monogr 48:111–126.
47.
Lucas JR, Brodin A, de Kort SR, Clayton NS (2004): Does hippocampal size correlate with the degree of caching specialization? Proc R Soc Lond B 271:2423–2429.
48.
McGregor A, Healy SD (1999): Spatial accuracy in food-storing and nonstoring birds. Anim Behav 58:727–734.
49.
Olson DJ, Kamil AC, Balda RP, Nims PJ (1995) Performance of 4 seed-caching corvid species in operant tests of nonspatial and spatial memory. J Comp Psychol 109:173–181.
50.
Poucet B, Buhot MC (1994): Effects of medial septal or unilateral hippocampal inactivations on reference and working spatial memory in rats. Hippocampus 4:315–321.
51.
Poucet B, Herrmann T, Buhot MC (1991): Effects of short-lasting inactivations of the ventral hippocampus and medial septum on long-term and short-term acquisition of spatial information in rats. Behav Brain Res 44:53–65.
52.
Pravosudov VV (2009): Development of spatial memory and the hippocampus under nutritional stress: adaptive priorities or developmental constraints in brain development; in Dukas R, Ratcliffe J (eds): Cognitive Ecology II. The Evolutionary Ecology of Learning, Memory and Information Use. Chicago, University of Chicago Press, pp 88–110.
53.
Pravosudov VV, Clayton NS (2002): A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapillus). Behav Neurosci 116:515–522.
54.
Pravosudov VV, de Kort SR (2006): Is the western scrub jay (Aphelocoma californica) really an underdog among food-caching corvids when it comes to hippocampal volume and food caching propensity? Brain Behav Evol 67:1–9.
55.
Rice NH, Martínez-Meyer E, Peterson AT (2003): Ecological niche differentiation in the Aphelocoma jays: a phylogenetic perspective. Biol J Linn Soc 80:369–383.
56.
Roth TC II, Brodin A, LaDage L, Smulders TV, Pravosudov VV (2010): Is bigger always better? A critical appraisal of the issue of volumetric analysis in the study of the hippocampus. Philos Trans R Soc Lond B Biol Sci 365:915–931.
57.
Roth TC II, LaDage LD, Freas CA, Pravosudov VV (2012): Variation in memory and the hippocampus across populations from different climates: a common garden approach. Proc Biol Sci 279:402–410.
58.
Roth TC II, Pravosudov VV (2009): Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc R Soc Lond B Biol Sci 276:401–405.
59.
Shapiro E, Wieraszko A (1996): Comparative, in vitro, studies of hippocampal tissue from homing and non-homing pigeons. Brain Res 725:199–206.
60.
Sherry DF (1984): Food storage by black-capped chickadees: memory for the location and contents of caches. Anim Behav 32:451–464.
61.
Sherry DF, Krebs JR, Cowie RJ (1981): Memory for the location of stored food in marsh tits. Anim Behav 29:1260–1266.
62.
Sherry DF, Vaccarino AL (1989): Hippocampus and memory for food caches in black-capped chickadees. Behav Neurosci 103:308–318.
63.
Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989): The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317.
64.
Shiflett MW, Gould KL, Smulders TV, DeVoogd TJ (2002): Septum volume and food-storing behavior are related in parids. J Neurobiol 51:215–222.
65.
Shiflett MW, Smulders TV, Benedict L, DeVoogd TJ (2003): Reversible inactivation of the hippocampal formation in food-storing black-capped chickadees (Poecile atricapillus). Hippocampus 13:437–444.
66.
Shiflett MW, Tomaszycki ML, Rankin AZ, DeVoogd TJ (2004): Long-term memory for spatial locations in a food-storing bird (Poecile atricapilla) requires activation of NMDA receptors in the hippocampal formation during learning. Behav Neurosci 118:121–130.
67.
Shimizu T, Bowers AN, Budzynski CA, Kahn MC, Bingman VP (2004): What does a pigeon (Columba livia) brain look like during homing? Selective examination of ZENK expression. Behav Neurosci 118:845–851.
68.
Siegel JJ, Nitz D, Bingman VP (2000): Hippocampal theta rhythm in awake and freely moving homing pigeons. Hippocampus 10:627–631.
69.
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.
70.
Smith HR, Pang KC (2005). Orexin-saporin lesions of the medial septum impair spatial memory. Neuroscience 132:261–271.
71.
Smulders TV, DeVoogd TJ (2000): The avian hippocampal formation and memory for hoarded food: spatial memory out in the real world; in Bolhuis JJ (ed): Brain, Perception, Memory: Advances in Cognitive Neuroscience. Oxford, Oxford University Press, pp 127–148.
72.
Smulders TV, Gould KL, Leaver LA (2010): Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals. Philos Trans R Soc Lond B Biol Sci 365:883–900.
73.
Smulders TV, Shiflett MW, Sperling AJ, DeVoogd TJ (2000): Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: the black-capped chickadee. J Neurobiol 44:414–422.
74.
Szekely AD (1999): The avian hippocampal formation: subdivisions and connectivity. Behav Brain Res 98:219–225.
75.
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.
76.
Turcek FJ, Kelso L (1968): Ecological aspects of food transportation and storage in the Corvidae. Commun Behav Biol Part A 1:227–297.
77.
Vander Wall SB (1982): An experimental analysis of cache recovery in Clark’s nutcracker. Anim Behav 30:84–94.
78.
Vander Wall SB, Balda RP (1981): Ecology and evolution of food-storage behavior in conifer-seed-caching corvids. Z Tierpsychol 56:217–242.
79.
Walsh TJ, Gandhi C, Stackman RW (1998): Reversible inactivation of the medial septum or nucleus basalis impairs working memory in rats: a dissociation of memory and performance. Behav Neurosci 112:1114–1124.
© 2013 S. Karger AG, Basel
2013
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.