Avian hippocampus: Recent advances in anatomy and physiological functions

Anacker, C., Luna, V.M., Stevens, G.S., Millette, A., Shores, R., Jimenez, J.C., et al., 2018. Hippocampal neurogenesis confers stress resilience by inhibiting the ventral dentate gyrus. Nature 559, 98–102.

Applegate, M.C., Gutnichenko, K.S., Mackevicius, E.L., Aronov, D., 2023. An entorhinal-like region in food-caching birds. Curr. Biol. 33, 2465–2477.

Armstrong, E.A., Richards-Rios, P., Addison, L., Sandilands, V., Guy, J.H., Wigley, P., et al., 2022. Poor body condition is associated with lower hippocampal plasticity and higher gut methanogen abundance in adult laying hens from two housing systems. Sci. Rep. 12, 15505.

Armstrong, E.A., Rufener, C., Toscano, M.J., Eastham, J.E., Guy, J.H., Sandilands, V., et al., 2020a. Keel bone fractures induce a depressive-like state in laying hens. Sci. Rep. 10, 3007.

Armstrong, E.A., Voelkl, B., Voegeli, S., Gebhardt-Henrich, S.G., Guy, J.H., Sandilands, V., et al., 2020b. Cell proliferation in the adult chicken hippocampus correlates with individual differences in time spent in outdoor areas and tonic immobility. Front. Vet. Sci. 7, 587.

Atoji, Y., Sarkar, S., Wild, J.M., 2016. Proposed homology of the dorsomedial subdivision and V-shaped layer of the avian hippocampus to Ammon's horn and dentate gyrus, respectively. Hippocampus 26, 1608–1617.

Atoji, Y., Wild, J.M., 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.

Atoji, Y., Wild, J.M., 2006. Anatomy of the avian hippocampal formation. Rev. Neurosci. 17, 3–15.

Atoji, Y., Wild, J.M., 2019. Projections of the densocellular part of the hyperpallium in the rostral Wulst of pigeons (Columba livia). Brain Res. 1711, 130–139.

Avigan, P.D., Cammack, K., Shapiro, M.L., 2020. Flexible spatial learning requires both the dorsal and ventral hippocampus and their functional interactions with the prefrontal cortex. Hippocampus 30, 733–744.

Azcoitia, I., Arevalo, M.A., De Nicola, A.F., Garcia-Segura, L.M., 2011. Neuroprotective actions of estradiol revisited. Trends Endocrinol. Metabol. 22, 467–473.

Bailey, D.J., Ma, C., Soma, K.K., Saldanha, C.J., 2013. Inhibition of hippocampal aromatization impairs spatial memory performance in a male songbird. Endocrinology 154, 4707–4714.

Bailey, D.J., Makeyeva, Y.V., Paitel, E.R., Pedersen, A.L., Hon, A.T., Gunderson, J.A., et al., 2017. Hippocampal aromatization modulates spatial memory and characteristics of the synaptic membrane in the male zebra finch. Endocrinology 158, 852–859.

Bailey, D.J., Rosebush, J.C., Wade, J., 2002. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J. Neurobiol. 52, 43–51.

Bailey, D.J., Saldanha, C.J., 2015. The importance of neural aromatization in the acquisition, recall, and integration of song and spatial memories in passerines. Horm. Behav. 74, 116–124.

Bannerman, D.M., Rawlins, J.N., McHugh, S.B., Deacon, R.M., Yee, B.K., Bast, T., et al., 2004. Regional dissociations within the hippocampus–memory and anxiety. Neurosci. Biobehav. Rev. 28, 273–283.

Bannerman, D.M., Sprengel, R., Sanderson, D.J., McHugh, S.B., Rawlins, J.N., Monyer, H., Seeburg, P.H., 2014. Hippocampal synaptic plasticity, spatial memory and anxiety. Nat. Rev. Neurosci. 15, 181–192.

Barha, C.K., Galea, L.A., 2010. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 1800, 1056–1067.

Barkan, S., Yom-Tov, Y., Barnea, A., 2014. A possible relation between new neuronal recruitment and migratory behavior in Acrocephalus warblers. Dev. Neurobiol. 74, 1194–1209.

Barnea, A., Nottebohm, F., 1994. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. USA 91, 11217–11221.

Baugh, A.T., Senft, R.A., Firke, M., Lauder, A., Schroeder, J., Meddle, S.L., et al., 2017. Risk-averse personalities have a systemically potentiated neuroendocrine stress axis: a multilevel experiment in Parus major. Horm. Behav. 93, 99–108.

Ben-Tov, M., Gutfreund, Y., 2022. Spatial cognition in birds. Curr. Biol. 32, R1085–R1089.

Bingman, V.P., Bagnoli, P., Ioali, P., Casini, G., 1984. Homing behaviour of pigeons after telencepahlic ablations. Brain Behav. Evol. 24, 94–108.

Bingman, V.P., Cheng, K., 2005. Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethol. Ecol. Evol. 17, 295–318.

Bingman, V.P., Erichsen, J.T., Anderson, J.D., Good, M.A., Pearce, J.M., 2006. Spared feature-structure discrimination but diminished salience of environmental geometry in hippocampal-lesioned homing pigeons (Columba livia). Behav. Neurosci. 120, 835–841.

Bingman, V.P., MacDougall-Shackleton, S.A., 2017. The avian hippocampus and the hypothetical maps used by navigating migratory birds (with some reflection on compasses and migratory restlessness). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 203, 465–474.

Biro, D., Meade, J., Guilford, T., 2004. Familiar route loyalty implies visual pilotage in the homing pigeon. Proc. Natl. Acad. Sci. USA 101, 17440–17443.

Bischof, H.J., Lieshoff, C., Watanabe, S., 2006. Spatial memory and hippocampal function in a non-foodstoring songbird, the zebra finch (Taeniopygia guttata). Rev. Neurosci. 17, 43–52.

Bouille, C., Bayle, J.D., 1978. Comparison between hypothalamic multiple-unit activity and corticotropic function after bilateral destruction of the hippocampus. Neuroendocrinology 25, 303–309.

Broadbent, N., Colombo, M., 2000. Visual and spatial discrimination behavior following hippocampal lesions in pigeons. Psychobiology 28, 463–475.

Brown, C.L.J., Zaytsoff, S.J.M., Iwaniuk, A.N., Metz, G.A.S., Montina, T., Inglis, G.D., 2023. Comparative analysis of the temporal impacts of corticosterone and simulated production stressors on the metabolome of broiler chickens. Metabolites 13, 144.

Bryant, K.G., Barker, J.M., 2020. Arbitration of approach-avoidance conflict by ventral hippocampus. Front. Neurosci. 14, 615337.

Buschman, T.J., Miller, E.K., 2014. Goal-direction and top-down control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369.

Chawla, M.K., Guzowski, J.F., Ramirez-Amaya, V., Lipa, P., Hoffman, K.L., Marriott, L.K., et al., 2005. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15, 579–586.

Chen, C.C., Winkler, C.M., Pfenning, A.R., Jarvis, E.D., 2013. Molecular profiling of the developing avian telencephalon: regional timing and brain subdivision continuities. J. Comp. Neurol. 521, 3666–3701.

Chen, X., Nelson, C.D., Li, X., Winters, C.A., Azzam, R., Sousa, A.A., et al., 2011. PSD-95 is required to sustain the molecular organization of the postsynaptic density. J. Neurosci. 31, 6329–6338.

Chen, Y., Liu, X., Li, S., Wan, H., 2018. Decoding pigeon behavior outcomes using functional connections among local field potentials. Comput. Intell. Neurosci. 2018, 3505371.

Cholvin, T., Hok, V., Giorgi, L., Chaillan, F.A., Poucet, B., 2018. Ventral midline thalamus is necessary for hippocampal place field stability and cell firing modulation. J. Neurosci. 38, 158–172.

Clayton, N.S., Krebs, J.R., 1994. Hippocampal growth and attrition in birds affected by experience. Proc. Natl. Acad. Sci. USA 91, 7410–7414.

Cnotka, J., Mohle, M., Rehkamper, G., 2008. Navigational experience affects hippocampus size in homing pigeons. Brain Behav. Evol. 72, 233–238.

Colombo, M., Broadbent, N.J., Taylor, C.S., Frost, N., 2001. The role of the avian hippocampus in orientation in space and time. Brain Res. 919, 292–301.

Coppola, V.J., Spencer, J.M., Peterson, R.M., Bingman, V.P., 2014. Hippocampal lesions in homing pigeons do not impair feature-quality or feature-quantity discrimination. Behav. Brain Res. 260, 83–91.

Danielson, N.B., Kaifosh, P., Zaremba, J.D., Lovett-Barron, M., Tsai, J., Denny, C.A., et al., 2016. Distinct contribution of adult-born hippocampal granule cells to context encoding. Neuron 90, 101–112.

Day, L.B., Guerra, M., Schlinger, B.A., Rothstein, S.I., 2008. Sex differences in the effects of captivity on hippocampus size in brown-headed cowbirds (Molothrus ater obscurus). Behav. Neurosci. 122, 527–534.

de Morais Magalhaes, N.G., Guerreiro Diniz, C., Guerreiro Diniz, D., Pereira Henrique, E., Correa Pereira, P.D., Matos Moraes, I.A., et al., 2017. Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla). PLoS One 12, e0179134.

Dickens, M., Romero, L.M., Cyr, N.E., Dunn, I.C., Meddle, S.L., 2009. Chronic stress alters glucocorticoid receptor and mineralocorticoid receptor mRNA expression in the European starling (Sturnus vulgaris) brain. J. Neuroendocrinol. 21, 832–840.

El-Falougy, H., Benuska, J., 2006. History, anatomical nomenclature, comparative anatomy and functions of the hippocampal formation. Bratisl. Lek. Listy 107, 103–106.

Erichsen, J.T., Bingman, V.P., Krebs, J.R., 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.

Ervin, K.S., Mulvale, E., Gallagher, N., Roussel, V., Choleris, E., 2015. Activation of the G protein-coupled estrogen receptor, but not estrogen receptor alpha or beta, rapidly enhances social learning. Psychoneuroendocrinology 58, 51–66.

Fusani, L., Gahr, M., Hutchison, J.B., 2001a. Aromatase inhibition reduces specifically one display of the ring dove courtship behavior. Gen. Comp. Endocrinol. 122, 23–30.

Fusani, L., Hutchison, J.B., Gahr, M., 2001b. Testosterone regulates the activity and expression of aromatase in the canary neostriatum. J. Neurobiol. 49, 1–8.

Gabor, C., Lymer, J., Phan, A., Choleris, E., 2015. Rapid effects of the G-protein coupled oestrogen receptor (GPER) on learning and dorsal hippocampus dendritic spines in female mice. Physiol. Behav. 149, 53–60.

Gagliardo, A., 2013. Forty years of olfactory navigation in birds. J. Exp. Biol. 216, 2165–2171.

Gagliardo, A., Bingman, V.P., 2024. The avian olfactory system and hippocampus: complementary roles in the olfactory and visual guidance of homing pigeon navigation. Curr. Opin. Neurobiol. 86, 102870.

Gagliardo, A., Cioccarelli, S., Giunchi, D., Pollonara, E., Colombo, S., Casini, G., Bingman, V.P., 2023. Deconstructing the flight paths of hippocampal-lesioned homing pigeons as they navigate near home offers insight into spatial perception and memory without a hippocampus. Behav. Brain Res. 436, 114073.

Gagliardo, A., Ioale, P., Savini, M., Dell'Omo, G., Bingman, V.P., 2009. Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur. J. Neurosci. 29, 2389–2400.

Gagliardo, A., Ioale, P., Savini, M., Lipp, H.P., Dell'Omo, G., 2007. Finding home: the final step of the pigeons' homing process studied with a GPS data logger. J. Exp. Biol. 210, 1132–1138.

Gagliardo, A., Pollonara, E., Coppola, V.J., Santos, C.D., Wikelski, M., Bingman, V.P., 2014. Evidence for perceptual neglect of environmental features in hippocampal-lesioned pigeons during homing. Eur. J. Neurosci. 40, 3102–3110.

Goodroe, S.C., Starnes, J., Brown, T.I., 2018. The complex nature of hippocampal-striatal interactions in spatial navigation. Front. Hum. Neurosci. 12, 250.

Gualtieri, F., Armstrong, E.A., Longmoor, G.K., D'Eath, R.B., Sandilands, V., Boswell, T., et al., 2019. Unpredictable chronic mild stress suppresses the incorporation of new neurons at the caudal pole of the chicken hippocampal formation. Sci. Rep. 9, 7129.

Guigueno, M.F., Snow, D.A., MacDougall-Shackleton, S.A., Sherry, D.F., 2014. Female cowbirds have more accurate spatial memory than males. Biol. Lett. 10, 20140026.

Guilford, T., Biro, D., 2014. Route following and the pigeon's familiar area map. J. Exp. Biol. 217, 169–179.

Gupta, S., Maurya, R., Saxena, M., Sen, J., 2012. Defining structural homology between the mammalian and avian hippocampus through conserved gene expression patterns observed in the chick embryo. Dev. Biol. 366, 125–141.

Hampton, R.R., Shettleworth, S.J., 1996. Hippocampal lesions impair memory for location but not color in passerine birds. Behav. Neurosci. 110, 831–835.

Healy, S.D., Gwinner, E., Krebs, J.R., 1996. Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav. Brain Res. 81, 61–68.

Healy, S.D., Krebs, J.R., 1992. Food storing and the hippocampus in corvids: amount and volume are correlated. Proc. R. Soc. A B 248, 241–245.

Herold, C., Bingman, V.P., Strockens, F., Letzner, S., Sauvage, M., Palomero-Gallagher, N., et al., 2014. Distribution of neurotransmitter receptors and zinc in the pigeon (Columba livia) hippocampal formation: a basis for further comparison with the mammalian hippocampus. J. Comp. Neurol. 522, 2553–2575.

Herold, C., Coppola, V.J., Bingman, V.P., 2015. The maturation of research into the avian hippocampal formation: recent discoveries from one of the nature's foremost navigators. Hippocampus 25, 1193–1211.

Herold, C., Schlomer, P., Mafoppa-Fomat, I., Mehlhorn, J., Amunts, K., Axer, M., 2019. The hippocampus of birds in a view of evolutionary connectomics. Cortex 118, 165–187.

Heyers, D., Musielak, I., Haase, K., Herold, C., Bolte, P., Gunturkun, O., et al., 2022. Morphology, biochemistry and connectivity of Cluster N and the hippocampal formation in a migratory bird. Brain Struct. Funct. 227, 2731–2749.

Hodgson, Z.G., Meddle, S.L., Christians, J.K., Sperry, T.S., Healy, S.D., 2008. Influence of sex steroid hormones on spatial memory in a songbird. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 194, 963–969.

Hodgson, Z.G., Meddle, S.L., Roberts, M.L., Buchanan, K.L., Evans, M.R., Metzdorf, R., et al., 2007. Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress. Proc. Biol. Sci. 274, 239–245.

Ito, H.T., 2018. Prefrontal-hippocampal interactions for spatial navigation. Neurosci. Res. 129, 2–7.

Jacobson, L., Sapolsky, R., 1991. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12, 118–134.

Jarvis, E.D., Gunturkun, O., Bruce, L., Csillag, A., Karten, H., Kuenzel, W., et al., 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci. 6, 151–159.

Jin, S.W., Lee, I., 2021. Differential encoding of place value between the dorsal and intermediate hippocampus. Curr. Biol. 31, 3053–3072 e3055.

Kadhim, H.J., Kang, S.W., Kuenzel, W.J., 2021. Possible roles of brain derived neurotrophic factor and corticotropin releasing hormone neurons in the nucleus of hippocampal commissure functioning within the avian neuroendocrine regulation of stress. Stress 24, 590–601.

Kahn, M.C., Hough 2nd, G.E., Ten Eyck, G.R., Bingman, V.P., 2003. Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study. J. Comp. Neurol. 459, 127–141.

Kahn, M.C., Siegel, J.J., Jechura, T.J., Bingman, V.P., 2008. Response properties of avian hippocampal formation cells in an environment with unstable goal locations. Behav. Brain Res. 191, 153–163.

Karten, H., Hodos, W., 1967. A stereotaxic atlas of the brain of the pigeon (Columba livia). Am. J. Psychol. 81, 1.

Kerr, J.N., de Kock, C.P., Greenberg, D.S., Bruno, R.M., Sakmann, B., Helmchen, F., 2007. Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex. J. Neurosci. 27, 13316–13328.

Kimball, M.G., Gautreaux, E.B., Couvillion, K.E., Kelly, T.R., Stansberry, K.R., Lattin, C.R., 2022. Novel objects alter immediate early gene expression globally for ZENK and regionally for c-Fos in neophobic and non-neophobic house sparrows. Behav. Brain Res. 428, 113863.

Kitaysky, A.S., Kitaiskaia, E.V., Piatt, J.F., Wingfield, J.C., 2003. Benefits and costs of increased levels of corticosterone in seabird chicks. Horm. Behav. 43, 140–149.

Knierim, J.J., 2015. The hippocampus. Curr. Biol. 25, R1116–R1121.

Krause, J.S., Perez, J.H., Chmura, H.E., Meddle, S.L., Hunt, K.E., Gough, L., et al., 2016. The stress response is attenuated during inclement weather in parental, but not in pre-parental, Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic. Horm. Behav. 83, 68–74.

Krause, J.S., Perez, J.H., Meddle, S.L., Wingfield, J.C., 2017. Effects of short-term fasting on stress physiology, body condition, and locomotor activity in wintering male white-crowned sparrows. Physiol. Behav. 177, 282–290.

Krause, J.S., Perez, J.H., Reid, A.M.A., Cheah, J., Bishop, V., Wingfield, J.C., et al., 2021. Acute restraint stress does not alter corticosteroid receptors or 11beta-hydroxysteroid dehydrogenase gene expression at hypothalamic-pituitary-adrenal axis regulatory sites in captive male white-crowned sparrows (Zonotrichia leucophrys gambelii). Gen. Comp. Endocrinol. 303, 113701.

Krebs, J.R., Sherry, D.F., Healy, S.D., Perry, V.H., Vaccarino, A.L., 1989. Hippocampal specialization of food-storing birds. Proc. Natl. Acad. Sci. USA 86, 1388–1392.

Kumar, A., Tamta, K., Arya, H., Maurya, R.C., 2023. Acute-stress induces the structural plasticity in hippocampal neurons of 15 and 30-day-old chick, Gallus gallus domesticus. Ann. Anat. 245, 151996.

LaDage, L.D., Roth 2nd, T.C., Fox, R.A., Pravosudov, V.V., 2010. Ecologically relevant spatial memory use modulates hippocampal neurogenesis. Proc. Biol. Sci. 277, 1071–1079.

LaDage, L.D., Roth 2nd, T.C., Pravosudov, V.V., 2011. Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.). Proc. Biol. Sci. 278, 138–143.

LaDage, L.D., Roth, T.C., Fox, R.A., Pravosudov, V.V., 2009. Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. Behav. Neurosci. 123, 284–291.

Lange, H., Walker, L., Orell, M., Smulders, T.V., 2022. Seasonal changes in the hippocampal formation of hoarding and non-hoarding tits. Learn. Beyond Behav. 50, 113–124.

Larosa, A., Wong, T.P., 2022. The hippocampus in stress susceptibility and resilience: reviewing molecular and functional markers. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 119, 110601.

Lattin, C.R., Kelly, T.R., Kelly, M.W., Johnson, K.M., 2022. Constitutive gene expression differs in three brain regions important for cognition in neophobic and non-neophobic house sparrows (Passer domesticus). PLoS One 17, e0267180.

Lee-Teng, E., Sherman, S.M., 1966. Memory consolidation of one-trial learning in chicks. Proc. Natl. Acad. Sci. USA 56, 926–931.

Li, M., Shang, Z., Zhao, K., Cheng, S., Wan, H., 2020. The role of Hp-NCL network in goal-directed routing information encoding of bird: a review. Brain Sci. 10, 617.

Loh, E., Kurth-Nelson, Z., Berron, D., Dayan, P., Duzel, E., Dolan, R., et al., 2017. Parsing the role of the hippocampus in approach-avoidance conflict. Cerebr. Cortex 27, 201–215.

Lormant, F., Cornilleau, F., Constantin, P., Meurisse, M., Lansade, L., Leterrier, C., et al., 2020. Research note: role of the hippocampus in spatial memory in Japanese quail. Poultry Sci. 99, 61–66.

Lucas, J.R., Brodin, A., de Kort, S.R., Clayton, N.S., 2004. Does hippocampal size correlate with the degree of caching specialization? Proc. Biol. Sci. 271, 2423–2429.

Luine, V.N., 2008. Sex steroids and cognitive function. J. Neuroendocrinol. 20, 866–872.

Madison, F.N., Bingman, V.P., Smulders, T.V., Lattin, C.R., 2024. A bird's eye view of the hippocampus beyond space: behavioral, neuroanatomical, and neuroendocrine perspectives. Horm. Behav. 157, 105451.

Mayer, U., Bischof, H.J., 2012. Brain activation pattern depends on the strategy chosen by zebra finches to solve an orientation task. J. Exp. Biol. 215, 426–434.

Mayer, U., Watanabe, S., Bischof, H.J., 2010. Hippocampal activation of immediate early genes Zenk and c-Fos in zebra finches (Taeniopygia guttata) during learning and recall of a spatial memory task. Neurobiol. Learn. Mem. 93, 322–329.

Mello, C.V., Kaser, T., Buckner, A.A., Wirthlin, M., Lovell, P.V., 2019. Molecular architecture of the zebra finch arcopallium. J. Comp. Neurol. 527, 2512–2556.

Mendez, P., Garcia-Segura, L.M., Muller, D., 2011. Estradiol promotes spine growth and synapse formation without affecting pre-established networks. Hippocampus 21, 1263–1267.

Milford, M., Schulz, R., 2014. Principles of goal-directed spatial robot navigation in biomimetic models. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130484.

Moaraf, S., Heiblum, R., Okuliarova, M., Hefetz, A., Scharf, I., Zeman, M., et al., 2021. Evidence that artificial light at night induces structure-specific changes in brain plasticity in a diurnal bird. Biomolecules 11, 1069.

Moaraf, S., Heiblum, R., Vistoropsky, Y., Okuliarova, M., Zeman, M., Barnea, A., 2020a. Artificial light at night increases recruitment of new neurons and differentially affects various brain regions in female zebra finches. Int. J. Mol. Sci. 21, 6140.

Moaraf, S., Vistoropsky, Y., Pozner, T., Heiblum, R., Okuliarova, M., Zeman, M., et al., 2020b. Artificial light at night affects brain plasticity and melatonin in birds. Neurosci. Lett. 716, 134639.

Montagnese, C.M., Krebs, J.R., Meyer, G., 1996. The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tissue Res. 283, 263–282.

Morandi-Raikova, A., Mayer, U., 2021. Selective activation of the right hippocampus during navigation by spatial cues in domestic chicks (Gallus gallus). Neurobiol. Learn. Mem. 177, 107344.

Morandi-Raikova, A., Mayer, U., 2022. Spatial cognition and the avian hippocampus: research in domestic chicks. Front. Psychol. 13, 1005726.

Morris, R.G., Garrud, P., Rawlins, J.N., O'Keefe, J., 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683.

Mouritsen, H., Heyers, D., Gunturkun, O., 2016. The neural basis of long-distance navigation in birds. Annu. Rev. Physiol. 78, 133–154.

Nikolakopoulou, A.M., Dermon, C.R., Panagis, L., Pavlidis, M., Stewart, M.G., 2006. Passive avoidance training is correlated with decreased cell proliferation in the chick hippocampus. Eur. J. Neurosci. 24, 2631–2642.

O'Keefe, J., Dostrovsky, J., 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175.

O'Leary, O.F., Cryan, J.F., 2014. A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol. Sci. 35, 675–687.

O'Neil, E.B., Newsome, R.N., Li, I.H., Thavabalasingam, S., Ito, R., Lee, A.C., 2015. Examining the role of the human hippocampus in approach-avoidance decision making using a novel conflict paradigm and multivariate functional magnetic resonance imaging. J. Neurosci. 35, 15039–15049.

Oberlander, J.G., Schlinger, B.A., Clayton, N.S., Saldanha, C.J., 2004. Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm. Behav. 45, 250–258.

Olafsdottir, H.F., Bush, D., Barry, C., 2018. The role of hippocampal replay in memory and planning. Curr. Biol. 28, R37–R50.

Patel, S.N., Clayton, N.S., Krebs, J.R., 1997. Spatial learning induces neurogenesis in the avian brain. Behav. Brain Res. 89, 115–128.

Payne, H.L., Lynch, G.F., Aronov, D., 2021. Neural representations of space in the hippocampus of a food-caching bird. Science 373, 343–348.

Pravosudov, V.V., 2003. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc. Biol. Sci. 270, 2599–2604.

Pravosudov, V.V., Clayton, N.S., 2001. Effects of demanding foraging conditions on cache retrival accuracy in food caching mountain chickadees (Poecile gambeli). Proc. R. Soc. B Biol. 268, 363–368.

Pravosudov, V.V., Clayton, N.S., 2002. A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav. Neurosci. 116, 515–522.

Pravosudov, V.V., Kitaysky, A.S., Omanska, A., 2006. The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison. Proc. R. Soc. Lond. B Biol. 273, 2641–2649.

Pravosudov, V.V., Omanska, A., 2005. Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees. J. Neurobiol. 62, 31–41.

Rattenborg, N.C., Martinez-Gonzalez, D., Roth 2nd, T.C., Pravosudov, V.V., 2011. Hippocampal memory consolidation during sleep: a comparison of mammals and birds. Biol. Rev. Camb. Phil. Soc. 86, 658–691.

Reboreda, J.C., Clayton, N.S., Kacelnik, A., 1996. Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport 7, 505–508.

Reiner, A., Perkel, D.J., Bruce, L.L., Butler, A.B., Csillag, A., Kuenzel, W., et al., 2004. The avian brain nomenclature forum: terminology for a new century in comparative neuroanatomy. J. Comp. Neurol. 473, E1–E6.

Robertson, B.A., Rathbone, L., Cirillo, G., D'Eath, R.B., Bateson, M., Boswell, T., et al., 2017. Food restriction reduces neurogenesis in the avian hippocampal formation. PLoS One 12, e0189158.

Rook, N., Stacho, M., Schwarz, A., Bingman, V.P., Gunturkun, O., 2023. Neuronal circuits within the homing pigeon hippocampal formation. J. Comp. Neurol. 531, 790–813.

Rosinha, M.U., Ferrari, E.A., Toledo, C.A., 2009. Immunohistochemical distribution of AMPA-type label in the pigeon (C. livia) hippocampus. Neuroscience 159, 438–450.

Roth 2nd, T.C., Stocker, K., Mauck, R., 2017. Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds. Dev. Neurobiol. 77, 93–101.

Sadananda, M., Bischof, H.J., 2004. c-fos is induced in the hippocampus during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata). Hippocampus 14, 19–27.

Saldanha, C.J., Remage-Healey, L., Schlinger, B.A., 2011. Synaptocrine signaling: steroid synthesis and action at the synapse. Endocr. Rev. 32, 532–549.

Saldanha, C.J., Schlinger, B.A., Micevych, P.E., Horvath, T.L., 2004. Presynaptic N-methyl-D-aspartate receptor expression is increased by estrogen in an aromatase-rich area of the songbird hippocampus. J. Comp. Neurol. 469, 522–534.

Saldanha, C.J., Tuerk, M.J., Kim, Y.H., Fernandes, A.O., Arnold, A.P., Schlinger, B.A., 2000. Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423, 619–630.

Salwiczek, L.H., Watanabe, A., Clayton, N.S., 2010. Ten years of research into avian models of episodic-like memory and its implications for developmental and comparative cognition. Behav. Brain Res. 215, 221–234.

Sandi, C., Rose, S.P., 1997. Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology (Berl) 133, 152–160.

Sapolsky, R.M., 2000. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch. Gen. Psychiatr. 57, 925–935.

Schaffer, A., Caicoya, A.L., Colell, M., Holland, R., von Fersen, L., Widdig, A., et al., 2021. Neophobia in 10 ungulate species-a comparative approach. Behav. Ecol. Sociobiol. 75, 102.

Senft, R.A., Meddle, S.L., Baugh, A.T., 2016. Distribution and abundance of glucocorticoid and mineralocorticoid receptors throughout the brain of the great Tit (Parus major). PLoS One 11, e0148516.

Sherry, D.F., Forbes, M.R., Khurgel, M., Ivy, G.O., 1993. Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc. Natl. Acad. Sci. USA 90, 7839–7843.

Sherry, D.F., Hoshooley, J.S., 2010. Seasonal hippocampal plasticity in food-storing birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 933–943.

Sherry, D.F., Vaccarino, A.L., Buckenham, K., Herz, R.S., 1989. The hippocampal complex of food-storing birds. Brain Behav. Evol. 34, 308–317.

Shimizu, T., Bowers, A.N., Budzynski, C.A., Kahn, M.C., Bingman, V.P., 2004. What does a pigeon (Columba livia) brain look like during homing? selective examination of ZENK expression. Behav. Neurosci. 118, 845–851.

Siegel, J.J., Nitz, D., Bingman, V.P., 2006. Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 16, 125–140.

Smulders, T.V., 2006. A multi-disciplinary approach to understanding hippocampal function in food-hoarding birds. Rev. Neurosci. 17, 53–69.

Smulders, T.V., 2017. The avian hippocampal formation and the stress response. Brain Behav. Evol. 90, 81–91.

Smulders, T.V., 2021. Telencephalic regulation of the HPA axis in birds. Neurobiol. Stress 15, 100351.

Smulders, T.V., DeVoogd, T.J., 2000. Expression of immediate early genes in the hippocampal formation of the black-capped chickadee (Poecile atricapillus) during a food-hoarding task. Behav. Brain Res. 114, 39–49.

Smulders, T.V., Shiflett, M.W., Sperling, A.J., DeVoogd, T.J., 2000. Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: the black-capped chickadee. J. Neurobiol. 44, 414–422.

Sosa, M., Giocomo, L.M., 2021. Navigating for reward. Nat. Rev. Neurosci. 22, 472–487.

Stacho, M., Herold, C., Rook, N., Wagner, H., Axer, M., Amunts, K., et al., 2020. A cortex-like canonical circuit in the avian forebrain. Science 369, eabc5534.

Striedter, G.F., 2016. Evolution of the hippocampus in reptiles and birds. J. Comp. Neurol. 524, 496–517.

Szekely, A.D., Krebs, J.R., 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.

Takeuchi, H., Yazaki, Y., Matsushima, T., Aoki, K., 1996. Expression of Fos-like immunoreactivity in the brain of quail chick emitting the isolation-induced distress calls. Neurosci. Lett. 220, 191–194.

Tarr, B.A., Rabinowitz, J.S., Ali Imtiaz, M., DeVoogd, T.J., 2009. Captivity reduces hippocampal volume but not survival of new cells in a food-storing bird. Dev. Neurobiol. 69, 972–981.

Taufique, S.K.T., Prabhat, A., Kumar, V., 2018a. Constant light environment suppresses maturation and reduces complexity of new born neuron processes in the hippocampus and caudal nidopallium of a diurnal corvid: implication for impairment of the learning and cognitive performance. Neurobiol. Learn. Mem. 147, 120–127.

Taufique, S.K.T., Prabhat, A., Kumar, V., 2018b. Illuminated night alters hippocampal gene expressions and induces depressive-like responses in diurnal corvids. Eur. J. Neurosci. 48, 3005–3018.

Taufique, S.T., Prabhat, A., Kumar, V., 2019. Light at night affects hippocampal and nidopallial cytoarchitecture: implication for impairment of brain function in diurnal corvids. J. Exp. Zool. A Ecol. Integr. Physiol. 331, 149–156.

Taziaux, M., Lopez, J., Cornil, C.A., Balthazart, J., Holloway, K.S., 2007. Differential c-fos expression in the brain of male Japanese quail following exposure to stimuli that predict or do not predict the arrival of a female. Eur. J. Neurosci. 25, 2835–2846.

Tobler, M., Sandell, M.I., 2007. Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm. Beyond Behav. 52, 640–645.

Tommasi, L., Gagliardo, A., Andrew, R.J., Vallortigara, G., 2003. Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus. Eur. J. Neurosci. 17, 1695–1702.

Treves, A., Tashiro, A., Witter, M.P., Moser, E.I., 2008. What is the mammalian dentate gyrus good for? Neuroscience 154, 1155–1172.

Tuscher, J.J., Taxier, L.R., Fortress, A.M., Frick, K.M., 2018. Chemogenetic inactivation of the dorsal hippocampus and medial prefrontal cortex, individually and concurrently, impairs object recognition and spatial memory consolidation in female mice. Neurobiol. Learn. Mem. 156, 103–116.

Vahaba, D.M., Remage-Healey, L., 2015. Brain estrogen production and the encoding of recent experience. Curr. Opin. Behav. Sci. 6, 148–153.

Watanabe, S., 1999. Effects of hippocampal lesions on spatial operant discrimination in pigeons. Behav. Brain Res. 103, 77–84.

Watanabe, S., Bischof, H.J., 2002. Spatial learning in songbird. Curr. Psychol. Lett. 3, 71–80.

Watanabe, S., Bischof, H.J., 2004. Effects of hippocampal lesions on acquisition and retention of spatial learning in zebra finches. Behav. Brain Res. 155, 147–152.

Wirt, R.A., Hyman, J.M., 2017. Integrating spatial working memory and remote memory: interactions between the medial prefrontal cortex and hippocampus. Brain Sci. 7, 43.

Witter, M.P., Kleven, H., Kobro Flatmoen, A., 2017. Comparative contemplations on the hippocampus. Brain Behav. Evol. 90, 15–24.

Zielinski, M.C., Shin, J.D., Jadhav, S.P., 2019. Coherent coding of spatial position mediated by theta oscillations in the hippocampus and prefrontal cortex. J. Neurosci. 39, 4550–4565.

Zimmer, C., Taff, C.C., Ardia, D.R., Rosvall, K.A., Kallenberg, C., Bentz, A.B., et al., 2023. Gene expression in the female tree swallow brain is associated with inter- and intra-population variation in glucocorticoid levels. Horm. Behav. 147, 105280.