The teleost fish hippocampal pallium, like the hippocampus of tetrapods, is essential for relational map-like spatial memories. In mammals, these relational memories involve the dynamic interactions among different hippocampal subregions and between the hippocampus-neocortex network, which performs specialized operations such as memory encoding and retrieval. However, how the teleost hippocampal homologue operates to achieve comparably sophisticated spatial cognition capabilities is largely unknown. In the present study, the progressive changes in the metabolic activity of the pallial regions that have been proposed as possible homologues of the mammalian hippocampus were monitored in goldfish. Quantitative cytochrome oxidase histochemistry was used to measure the level of activation along the rostrocaudal axis of the ventral (Dlv) and dorsal parts of the dorsolateral division (Dld) and in the dorsoposterior division (Dp) of the goldfish telencephalic pallium throughout the time course of the learning process of a spatial memory task. The results revealed a significant increase in spatial memory-related metabolic activity in the Dlv, but not in the Dld, suggesting that the Dlv, but not the Dld, is comparable to the amniote hippocampus. Regarding the Dlv, the level of activation of the precommissural Dlv significantly increased at training onset but progressively declined to finally return to the basal pretraining level when the animals mastered the spatial task. In contrast, the commissural Dlv activation persisted even when the acquisition phase was completed and the animal's performance reached an asymptotic level. These results suggest that, like the dentate gyrus of mammals, the goldfish precommissural Dlv seems to respond nonlinearly to increments of change in sensory input, performing pattern separation under highly dissimilar input patterns. In addition, like the CA3 of mammals, the commissural Dlv likely operates in a continuum between two modes, a pattern separation or storage operation mode at early acquisition when the change in the sensory input is high, probably driven by the precommissural Dlv output, and a pattern completion or recall operation mode when the animals have mastered the task and the change in sensory input is small. Finally, an unexpected result of the present study is the persistent activation of the area Dp throughout the complete spatial task training period, which suggests that the Dp could be an important component of the pallial network involved in spatial memory in goldfish, and supports the hypothesis proposing that the Dp is a specialized part of the hippocampal pallium network.

1.
Abellán A, Desfilis E, Medina L (2014): Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front Neuroanat 4:8-59.
2.
Aggleton JP, Kyda RJ, Bilkey DK (2004): When is the perirhinal cortex necessary for the performance of spatial memory tasks? Neurosci Biobehav Rev 28:611-624.
3.
Aggleton JP, Vann SD, Oswald CJP, Good M (2000): Identifying cortical inputs to the rat hippocampus that subserve allocentric spatial processes: a simple problem with a complex answer. Hippocampus 10:466-474.
4.
Allen TA, Fortin NJ (2013): The evolution of episodic memory. Proc Natl Acad Sci USA 110 (suppl 2):10379-10386.
5.
Amaral D, Lavenex P (2007): Hippocampal neuroanatomy; in Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J (eds): The Hippocampus Book. Oxford, Oxford University Press.
6.
Atoji Y, Sarkar S, Wild JM (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.
7.
Atoji Y, Wild JM (2006): Anatomy of the avian hippocampal formation. Rev Neurosci 17:3-15.
8.
Atoji Y, Wild JM (2014): Efferent and afferent connections of the olfactory bulb and prepiriform cortex in the pigeon (Columba livia). J Comp Neurol 522:1728-1752.
9.
Auger SD, Zeidman P, Maguire EA (2015): A central role for the retrosplenial cortex in de novo environmental learning. Elife 18:4.
10.
Biechl D, Tietje K, Ryu S, Grothe B, Gerlach G, Wullimann MF (2017): Identification of accessory olfactory system and medial amygdala in the zebrafish. Sci Rep 7:44295.
11.
Bingman VP, Sharp PE (2006): Neuronal implementation of hippocampal-mediated spatial behavior: a comparative evolutionary perspective. Behav Cogn Neurosci Rev 5:80-91.
12.
Blumhagen F, Zhu P, Shum J, Schärer YP, Yaksi E, Deisseroth K, Friedrich RW (2011): Neuronal filtering of multiplexed odour representations. Nature 479:493-498.
13.
Bontempi B, Laurent-Demir C, Destrade C, Jaffard R (1999): Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400:671-675.
14.
Broglio C, Rodríguez F, Gómez A, Arias JL, Salas C (2010): Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210:191-201.
15.
Burgess, N, Maguire, EA, O'Keefe J (2002): The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
16.
Butler AB (2000): Topography and topology of the teleost telencephalon: a paradox resolved. Neurosci Lett 293:95-98.
17.
Butler AB, Hodos W (2005): Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, ed 2. Hoboken, Wiley.
18.
Buzsáki G, Moser EI (2013): Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130-138.
19.
Chadwick MJ, Jolly AE, Amos DP, Hassabis D, Spiers HJ (2015): A goal direction signal in the human entorhinal/subicular region. Curr Biol 25:87-92.
20.
Churchwell JC, Morris AM, Musso ND, Kesner RP (2010): Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol Learn Mem 93:415-421.
21.
Clark RE, Squire LR (2013): Similarity in form and function of the hippocampus in rodents, monkeys, and humans. Proc Natl Acad Sci USA 110:10365-10370.
22.
Colombo M, Broadbent N (2000): Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neurosci Biobehav Rev 24:465-484.
23.
Conejo NM, Cimadevilla JM, González-Pardo H, Méndez-Couz M, Arias JL (2013): Hippocampal inactivation with TTX impairs long-term spatial memory retrieval and modifies brain metabolic activity. PLoS One 8:e64749.
24.
Conejo NM, González-Pardo H, Gonzalez-Lima F, Arias JL (2010): Spatial learning of the water maze: progression of brain circuits mapped with cytochrome oxidase histochemistry. Neurobiol Learn Mem 93:362-371.
25.
Demski LS (2003): In a fish's brain´s eye: visual pallium of teleosts; in Collin SP, Marshall NJ (eds): Sensory Processing in Aquatic Environments. New York, Springer.
26.
Demski LS (2013): The pallium and mind/behavior relationships in teleost fishes. Brain Behav Evol 82:31-44.
27.
Dirian L, Galant S, Coolen M, Chen W, Bedu S, Houart C, Bally-Cuif L, Foucher I (2014): Spatial regionalization and heterochrony in the formation of adult pallial neural stem cells. Dev Cell 30:123-136.
28.
Durán E, Ocaña FM, Broglio C, Rodríguez F, Salas C (2010): Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a “hole-board” task. Behav Brain Res 214:480-487.
29.
Durán, E, Ocaña FM, Gómez A, Jiménez-Moya F, Broglio C, Rodríguez F, Salas C (2008): Telencephalon ablation impairs goldfish allocentric spatial learning in a “holeboard” task. Acta Neurobiol Exp 68:519-525.
30.
Eichenbaum H (2004): Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44:109-120.
31.
Eichenbaum H, Sauvage M, Fortin N, Komorowski R, Lipton P (2012): Towards a functional organization of episodic memory in the medial temporal lobe. Neurosci Biobehav Rev 36:1597-1608.
32.
Eichenbaum H, Schoenbaum G, Young B, Bunsey M (1996): Functional organization of the hippocampal memory system. Proc Natl Acad Sci USA 93:13500-13507.
33.
Elliott SB, Harvey-Girard E, Giassi AC, and Maler L (2017): Hippocampal-like circuitry in the pallium of an electric fish: possible substrates for recursive pattern separation and completion. J Comp Neurol 525:8-46.
34.
Epstein RA, Vass LK (2014): Neural systems for landmark-based wayfinding in humans. Philos Trans R Soc Lond B Biol Sci 369:20120533.
35.
Finger TE (1975): The distribution of the olfactory tracts in the bullhead catfish, Ictalurus nebulosus. J Comp Neurol 161:125-141.
36.
Folgueira M, Bayley P, Navratilova P, Becker TS, Wilson SW, Clarke JD (2012): Morphogenesis underlying the development of the everted teleost telencephalon. Neural Dev 7:32.
37.
Galani R, Weiss I, Cassel JC, Kelche C (1998): Spatial memory, habituation, and reactions to spatial and nonspatial changes in rats with selective lesions of the hippocampus, the entorhinal cortex or the subiculum. Behav Brain Res 96:1-12.
38.
Ganz J, Kaslin J, Hochmann S, Freudenreich D, Brand M (2010): Heterogeneity and Fgf dependence of adult neural progenitors in the zebrafish telencephalon. Glia 58:1345-1363.
39.
Ganz J, Kroehne V, Freudenreich D, Machate A, Geffarth M, Braasch I, Kaslin J, Brand M (2014): Subdivisions of the adult zebrafish pallium based on molecular marker analysis. F1000Res 3:308.
40.
Gonzalez-Lima F, Cada A (1994): Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience 63:559-578.
41.
Gonzalez-Lima F, Jones D (1994): Quantitative mapping of cytochrome oxidase activity in the central auditory system of the gerbil: a study with calibrated activity standards and metal-intensified histochemistry. Brain Res 660:34-49.
42.
Good M, Honey RC (1997): Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111:487-493.
43.
Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006): Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263-277.
44.
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.
45.
Guzowski JF, Knierim JJ, Moser EI (2004): Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 44:581-584.
46.
Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005): Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
47.
Hartley T, Lever C, Burgess N, O'Keefe J (2014): Space in the brain: how the hippocampal formation supports spatial cognition. Philos Trans R Soc Lond B Biol Sci 369:20120510.
48.
Herold C, Coppola VJ, Bingman VP (2015): The maturation of research into the avian hippocampal formation: recent discoveries from one of the nature's foremost navigators. Hippocampus 25:1193-1211.
49.
Hevner RF, Liu S, Wong-Riley MTT (1995): A metabolic map of cytochrome oxidase in the rat brain: histochemical, densitometric and biochemical studies. Neuroscience 65:313-342.
50.
Holding ML, Frazier JA, Taylor EN, Strand CR (2012): Experimentally altered navigational demands induce changes in the cortical forebrain of free-ranging northern pacific rattlesnakes (Crotalus o. oreganus). Brain Behav Evol 79:144-154.
51.
Holmes PH, Northcutt RG (2003): Connections of the pallial telencephalon in the Senegal bichir, Polypterus. Brain Behav Evol 61:113-147.
52.
Holmgren N (1922): Points of view concerning forebrain morphology in lower vertebrates. J Comp Neurol 34:491-459.
53.
Ingle D, Sahagian D (1973): Solution of a spatial constancy problem by goldfish. Physiol Psychol 1:83-84.
54.
Insausti R, Marcos P, Arroyo-Jimenez MM, Blaizot X, Martinez-Marcos A (2002): Comparative aspects of the olfactory portion of the entorhinal cortex and its projection to the hippocampus in rodents, nonhuman primates, and the human brain. Brain Res Bull 57:557-560.
55.
Ito H, Yamamoto N (2009): Non-laminar cerebral cortex in teleost fishes? Biol Lett 5:117-121.
56.
Jacobs LF (2012): From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci USA 109:10693-10700.
57.
Kempermann G (2012): New neurons for “survival of the fittest”. Nat Rev Neurosci 13:727-736.
58.
Kesner RP, Rolls ET (2015): A computational theory of hippocampal function, and tests of the theory: new developments. Neurosci Biobehav Rev 48:92-147.
59.
Kohonen T (1984): Self-Organization and Associative Memory. Berlin, Springer.
60.
Kroehne V, Freudenreich D, Hans S, Kaslin J, Brand M (2011): Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development 38:4831-4841.
61.
Kubik S, Miyashita T, Guzowski JF (2007): Using immediate-early genes to map hippocampal subregional functions. Learn Mem 14:758-770.
62.
Lacy JW, Yassa MA, Stark SM, Muftuler LT, Stark CE (2011): Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high resolution fMRI and variable mnemonic similarity. Learn Mem 18:15-18.
63.
Lavenex P, Suzuki WA, Amaral DG (2004): Perirhinal and parahippocampal cortices of the macaque monkey: intrinsic projections and interconnections. J Comp Neurol 472:371-394.
64.
Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004): Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456-459.
65.
Leutgeb S, Leutgeb JK (2007): Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14:745-757.
66.
Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007): Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
67.
Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004): Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295-1298.
68.
Levine RL, Dethier S (1985): The connections between the olfactory bulb and the brain in the goldfish. J Comp Neurol 237:427-444.
69.
Lohman AHM, Smeets WJAJ (1993): Overview of the main and accessory olfactory bulb projections in reptiles. Brain Behav Evol 41:147-155.
70.
López JC, Bingman VP, Rodríguez F, Gómez Y, Salas C (2000a): Dissociation of place and cue learning by telencephalic ablation in goldfish. Behav Neurosci 114:687-699.
71.
López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (1999): Multiple spatial learning strategies in goldfish (Carassius auratus). Anim Cogn 2:109-120.
72.
López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (2000b): Reversal learning deficit in a spatial task but not in a cued one after telencephalic ablation in goldfish. Behav Brain Res 109:91-98.
73.
López JC, Vargas JP, Gómez Y, Salas C (2003): Spatial and non-spatial learning in turtles: the role of medial cortex. Behav Brain Res 143:109-120.
74.
Manns JR, Eichenbaum H (2006): Evolution of declarative memory. Hippocampus 16:795-808.
75.
Matrov D, Kolts I, Harro J (2007): Cerebral oxidative metabolism in rats with high and low exploratory activity. Neurosci Lett 413:154-158.
76.
McClelland JL, McNaughton BL, O'Reilly RC (1995): Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457.
77.
McNaughton BL, Morris RG (1987): Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408-415.
78.
Méndez-López M, Arias JL, Bontempi B, Wolff M (2013): Reduced cytochrome oxidase activity in the retrosplenial cortex after lesions to the anterior thalamic nuclei. Behav Brain Res 250:264-273.
79.
Moscovitch M, Cabeza R, Winocur G, Nadel L (2016): Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol 67:105-134.
80.
Moser EI, Kropff E, Moser MB (2008): Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31:69-89.
81.
Mueller T, Wullimann MF (2009): An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav Evol 74:30-42.
82.
Mullally SL, Maguire EA (2011): A new role for the parahippocampal cortex in representing space. J Neurosci 31:7441-7449.
83.
Myers CE, Scharfman HE (2011): Pattern separation in the dentate gyrus: a role for the CA3 backprojection. Hippocampus 21:1190-1215.
84.
Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD, Kato A, Carr CA, Johnston D, Wilson MA, Tonegawa S (2002): Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297:211-218.
85.
Nieuwenhuys R (1963): The comparative anatomy of the actinopterygian forebrain. J Hirnforsch 13:171-192.
86.
Nieuwenhuys R (1969): A survey of the structure of the forebrain in higher bony fishes (Osteichthyes). Ann NY Acad Sci 167:31-64.
87.
Nieuwenhuys R (2009): The forebrain of actinopterygians revisited. Brain Behav Evol 73:229-252.
88.
Nieuwenhuys R (2011): The development and general morphology of the telencephalon of actinopterygian fishes: synopsis, documentation and commentary. Brain Struct Funct 215:141-157.
89.
Nikonov AA, Caprio J (2007): Responses of olfactory forebrain units to amino acids in the channel catfish. J Neurophysiol 97:2490-2498.
90.
Nikonov AA, Finger TE, Caprio J (2005): Beyond the olfactory bulb: an odotopic map in the forebrain. Proc Natl Acad Sci USA 102:18688-18693.
91.
Northcutt RG (2006): Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494:903-943.
92.
Northcutt RG, Davis RE (1983): Telencephalic organization in rayfinned fishes; in Davis RE, Northcutt RG (eds): Fish Neurobiology. Ann Arbor, University of Michigan Press, vol 2.
93.
Northcutt RG, Braford MR Jr (1980): New observation on the organization and evolution of the telencephalon of the actinopterygian fishes; in Ebbeson SOE (ed): Comparative Neurology of the Telencephalon. New York, Plenum Press.
94.
Ocaña FM, Gómez A, Durán E, Martín Monzón I, Trujillo I, Broglio C, Rodríguez F, Salas C (2016): Voltage-Sensitive Dye Imaging Reveals Segregated Sensory Areas and Topographic Maps in the Goldfish Pallium (Abstract Book). Munich, 8th European Conference on Comparative Neurobiology, p 47.
95.
O'Keefe J, Nadel L (1978): The Hippocampus as a Cognitive Map. Oxford, Clarendon Press.
96.
Oswald CJ, Good M (2000): The effects of combined lesions of the subicular complex and the entorhinal cortex on two forms of spatial navigation in the water maze. Behav Neurosci 114:211-217.
97.
Papp G, Witter MP, Treves A (2016): The CA3 network as a memory store for spatial representations. Learn Mem 14:732-744.
98.
Parron C, Save E (2004): Comparison of the effects of entorhinal and retrosplenial cortical lesions on habituation, reaction to spatial and non-spatial changes during object exploration in the rat. Neurobiol Learn Mem 82:1-11.
99.
Poirier GL, Amin E, Aggleton JP (2008): Qualitatively different hippocampal subfield engagement emerges with mastery of a spatial memory task by rats. J Neurosci 28:1034-1045.
100.
Poremba A, Jones D, Gonzalez-Lima F (1998): Classical conditioning modifies cytochrome oxidase activity in the auditory system. Eur J Neurosci 10:3035-3043.
101.
Portavella M, Torres B, Salas C (2004): Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 9:2335-2342.
102.
Prechtl JC, von der Emde G, Wolfart J, Karamürsel S, Akoev GN, Andrianov YN, Bullock TH (1998): Sensory processing in the pallium of a mormyrid fish. J Neurosci 18:7381-7393.
103.
Reiner A, Karten HJ (1985): Comparison of olfactory bulb projections in pigeons and turtles. Brain Behav Evol 27:11-27.
104.
Rodríguez F, Durán E, Vargas J, Torres B, Salas C (1994): Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes. Anim Learn Behav 22:409-420.
105.
Rodríguez F, Lopez JC, Vargas JP, Gomez Y, Broglio C, Salas C (2002): Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 22:2894-2903.
106.
Rodríguez-Expósito B, Gómez A, Martín-Monzón I, Reiriz M, Rodríguez F, Salas C (2017): Goldfish hippocampal pallium is essential to associate temporally discontiguous events. Neurobiol Learn Mem 139:128-134.
107.
Rolls ET (2013): The mechanisms for pattern completion and pattern separation in the hippocampus. Front Syst Neurosci 7:74.
108.
Rolls ET (2016): Pattern separation, completion, and categorisation in the hippocampus and neocortex. Neurobiol Learn Mem 129:4-28.
109.
Rolls ET, Treves A (1998): Neural Networks and Brain Function. Oxford, Oxford University Press.
110.
Room P, Groenewegen HJ, Lohman AH (1984): Inputs from the olfactory bulb and olfactory cortex to the entorhinal cortex in the cat. 1. Anatomical observations. Exp Brain Res 56:488-496.
111.
Ros J, Pellerin L, Magara F, Dauguet J, Schenk F, Magistretti PJ (2006): Metabolic activation pattern of distinct hippocampal subregions during spatial learning and memory retrieval. J Cereb Blood Flow Metab 26:468-477.
112.
Ross RS, Eichenbaum H (2006): Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J Neurosci 26:4852-4859.
113.
Saidel WM, Marquez-Houston K, Butler AB (2001): Identification of visual pallial telencephalon in the goldfish, Carassius auratus: a combined cytochrome oxidase and electrophysiological study. Brain Res 919:82-93.
114.
Salas C, Broglio C, Durán E, Ocaña FM, Martín-Monzón I, Gómez A, Rodríguez F (2017): Spatial Learning and Its Neural Basis in Fish: Reference Module in Neuroscience and Biobehavioral Psychology. Amsterdam, Elsevier.
115.
Salas C, Broglio C, Rodriguez F (2003): Evolution of forebrain and spatial cognition in vertebrates: conservation across diversity. Brain Behav Evol 62:72-82.
116.
Salas C, Broglio C, Rodríguez F, López JC, Portavella M, Torres B (1996a): Telencephalic ablation in goldfish impairs performance in a spatial constancy problem but not in a cued one. Behav Brain Res 79:193-200.
117.
Salas C, Rodríguez F, Vargas JP, Durán E, Torres B (1996b): Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. Behav Neurosci 110:965-980.
118.
Schenk F, Morris RGM (1985): Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Exp Brain Res 109:195-206.
119.
Sherry D, Duff S (1996): Behavioural and neural bases of orientation in food-storing birds. J Exp Biol 199:165-172.
120.
Shimizu T, Cox K, Karten HJ (1995): Intratelencephalic projections of the visual Wulst in pigeons (Columba livia). J Comp Neurol 359:551-572.
121.
Shipley MY, Ennis M, Puche A (2004): Olfactory system; in Paxinos G (ed): The Rat Nervous System, ed 3. Amsterdam, Elsevier.
122.
Sotelo MI, Daneri MF, Bingman VP, Muzio RN (2016): Telencephalic neuronal activation associated with spatial memory in the terrestrial toad Rhinella arenarum: participation of the medial pallium during navigation by geometry. Brain Behav Evol 88:149-160.
123.
Squire LR (2004): Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171-177.
124.
Squire LR, Stark CE, Clark RE (2004): The medial temporal lobe. Annu Rev Neurosci 27:279-330.
125.
Steffenach HA, Witter M, Moser MB, Moser EI (2005): Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313.
126.
Striedter GF (2016): Evolution of the hippocampus in reptiles and birds. J Comp Neurol 524:496-517.
127.
Suzuki WA, Amaral DG (1994): Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol 350:497-533.
128.
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.
129.
Treves A, Rolls ET (1994): A computational analysis of the role of the hippocampus in memory. Hippocampus 4:374-391.
130.
Trinh AT, Harvey-Girard E, Teixeira F, Maler L (2016): Cryptic laminar and columnar organization in the dorsolateral pallium of a weakly electric fish. J Comp Neurol 524:408-428.
131.
Uceda S, Ocaña FM, Martín-Monzón I, Rodríguez-Expósito B, Durán E, Rodríguez F (2015): Spatial learning-related changes in metabolic brain activity contribute to the delimitation of the hippocampal pallium in goldfish. Behav Brain Res 292:403-408.
132.
Vargas JP, Bingman VP, Portavella M, López JC (2006): Telencephalon and geometric space in goldfish. Eur J Neurosci 24:2870-2878.
133.
Vargas JP, López JC, Salas C, Thinus-Blanc C (2004): Encoding of geometric and featural spatial information by goldfish (Carassius auratus). J Comp Psychol 118:206-216.
134.
Vargas JP, Rodriguez F, Lopez JC, Arias JL, Salas C (2000): Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish. Brain Res 865:77-84.
135.
Vazdarjanova A, Guzowski JF (2004): Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489-6496.
136.
von Bartheld CS, Meyer DL, Fiebig E, Ebbesson SO (1984): Central connections of the olfactory bulb in the goldfish, Carassius auratus. Cell Tissue Res 238:475-487.
137.
Wallace MN (1987): Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex. Brain Res 418:178-182.
138.
Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000): Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Sci 911:1-24.
139.
Wong-Riley MT (1989): Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94-101.
140.
Wullimann MF (2009): Secondary neurogenesis and telencephalic organization in zebrafish and mice: a brief review. Int Zool 4:123-133.
141.
Wullimann MF, Mueller T (2004): Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143-162.
142.
Yaksi E, von Saint Paul F, Niessing J, Bundschuh ST, Friedrich RW (2009): Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 12:474-482.
143.
Yamamoto N, Ishikawa Y, Yoshimoto M, Xue HG, Bahaxar N, Sawai N (2007): A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain Behav Evol 69:96-104.
144.
Yamamoto N, Ito H (2005): Fiber connections of the anterior preglomerular nucleus in cyprinids with notes on telencephalic connections of the preglomerular complex. J Comp Neurol 491:212-233.
145.
Yamamoto N, Ito H (2008): Visual, lateral line, and auditory ascending pathways to the dorsal telencephalic area through the rostrolateral region of the lateral preglomerular nucleus in cyprinids. J Comp Neurol 508:615-647.
146.
Yassa MA, Stark C (2011): Pattern separation in the hippocampus. Trends Neurosci 34:515-525.
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