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9 - Relational Memory Functions of the Hippocampal Pallium in Teleost Fish

from Part I - Evolution of Learning Processes

Published online by Cambridge University Press:  26 May 2022

Mark A. Krause
Affiliation:
Southern Oregon University
Karen L. Hollis
Affiliation:
Mount Holyoke College, Massachusetts
Mauricio R. Papini
Affiliation:
Texas Christian University
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Summary

The hippocampus of mammals, birds, reptiles, and amphibians is a fundamental brain structure for certain forms of relational memory. We review here the experimental evidence indicating that the hippocampal pallium of teleost fish, like the hippocampus of land vertebrates, is involved in relational map-like spatial memory, endowing fish behavior with the capability for allocentric navigation and allowing the flexible expression of spatial memory. In addition, recent evidence suggests that the teleost fish hippocampal pallium plays an important role in the processing of the temporal dimensions of relational memory. The functional similarities in the hippocampal pallium of taxa that diverged millions of years ago suggest the possibility that some features of the hippocampal networks allowing the processing of the spatial as well the temporal dimensions of relational associative memories appeared early in vertebrate evolution and were conserved through phylogenesis.

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Publisher: Cambridge University Press
Print publication year: 2022

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References

Aggleton, J. P., & Brown, M. W. (1999). Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioral and Brain Sciences, 22(03), 425444. https://doi.org/10.1017/S0140525X99002034Google Scholar
Allen, T. A., & Fortin, N. J. (2013). The evolution of episodic memory. Proceedings of the National Academy of Sciences, 110(Supplement 2), 1037910386. https://doi.org/10.1073/pnas.1301199110CrossRefGoogle ScholarPubMed
Bingman, V. P., Riters, L. V., Strasser, R., & Gagliardo, A. (1998). Neuroethology of avian navigation. In Balda, R. P., Pepperberg, I. M., & Kamil, A. C. (Eds.), Animal cognition in nature (pp. 201226). Academic Press. https://doi.org/10.1016/b978-012077030-4/50059-3Google Scholar
Bird, C. M., & Burgess, N. (2008). The hippocampus and memory: Insights from spatial processing. Nature Reviews Neuroscience, 9(3), 182194. https://doi.org/10.1038/nrn2335Google Scholar
Broglio, C., Gómez, A., Durán, E., Salas, C., & Rodríguez, F. (2011). Brain and cognition in teleost fish. In Brown, C., Laland, K., & Krause, J. (Eds.), Fish cognition and behavior (pp. 325358). Wiley. https://doi.org/10.1002/9781444342536.ch15Google Scholar
Broglio, C., Rodríguez, F., Gómez, A., Arias, J. L., & Salas, C. (2010). Selective involvement of the goldfish lateral pallium in spatial memory. Behavioural Brain Research, 210(2), 191201. https://doi.org/10.1016/j.bbr.2010.02.031Google Scholar
Broglio, C., Rodríguez, F., & Salas, C. (2003). Spatial cognition and its neural basis in teleost fishes. Fish and Fisheries, 4(3), 247255. https://doi.org/10.1046/j.1467-2979.2003.00128.xGoogle Scholar
Burgess, N. (2008). Spatial cognition and the brain. Annals of the New York Academy of Sciences, 1124, 7797. https://doi.org/10.1196/annals.1440.002Google Scholar
Burgess, N., Maguire, E., & O’Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625641. https://doi.org/10.1016/S0896-6273(02)00830-9Google Scholar
Butler, A. B. (2000). Topography and topology of the teleost telencephalon: A paradox resolved. Neuroscience Letters, 293(2), 9598. https://doi.org/10.1016/S0304-3940(00)01497-XGoogle Scholar
Butler, A. B., & Hodos, W. (2005). Comparative vertebrate neuroanatomy. John Wiley & Sons. https://doi.org/10.1002/0471733849Google Scholar
Buzsáki, G., & Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neuroscience, 16(2), 130138. https://doi.org/10.1038/nn.3304Google Scholar
Cheng, K. (1986). A purely geometric module in the rat’s spatial representation. Cognition, 23(2), 149178. https://doi.org/10.1016/0010-0277(86)90041-7Google Scholar
Cheng, K. (1994). The determination of direction in landmark-based spatial search in pigeons: A further test of the vector sum model. Animal Learning & Behavior, 22, 291301. https://doi.org/10.3758/BF03209837Google Scholar
Cheng, K., & Gallistel, C. R. (1984). Testing the geometric power of an animal’s spatial representation. In Roitblat, H. L., Terrace, H.S., & Bever, T. G. (Eds.), Animal cognition (pp. 409423). Erlbaum. https://doi.org/10.4324/9781315802602Google Scholar
Chersi, F., & Burgess, N. (2015). The cognitive architecture of spatial navigation: Hippocampal and striatal contributions. Neuron, 88(1), 6477. https://doi.org/10.1016/j.neuron.2015.09.021Google Scholar
Clark, R. E., & Squire, L. R. (1998). Classical conditioning and brain systems: The role of awareness. Science, 280, 7781. https://doi.org/10.1126/science.280.5360.77Google Scholar
Clark, R. E., & Squire, L. R. (2013). Similarity in form and function of the hippocampus in rodents, monkeys, and humans. Proceedings of the National Academy of Sciences, 110(Supplement 2), 1036510370. https://doi.org/10.1073/pnas.1301225110Google Scholar
Clayton, N., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395, 272274. https://doi.org/10.1038/26216Google Scholar
Cohen, N. J., & Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system. MIT Press. ISBN: 9780262032032.Google Scholar
Colombo, M., & Broadbent, N. (2000). Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neuroscience and Biobehavioral Reviews, 24(4), 465484. https://doi.org/10.1016/S0149-7634(00)00016-6Google Scholar
Conejo, N. M., González-Pardo, H., Gonzalez-Lima, F., & Arias, J. L. (2010). Spatial learning of the water maze: Progression of brain circuits mapped with cytochrome oxidase histochemistry. Neurobiology of Learning and Memory, 93(3), 362371. https://doi.org/10.1016/j.nlm.2009.12.002Google Scholar
Costa, S. S., Andrade, R., Carneiro, L. A., Gonçalves, E. J., Kotrschal, K., & Oliveira, R. F. (2011). Sex differences in the dorsolateral telencephalon correlate with home range size in blenniid fish. Brain, Behavior and Evolution, 77(1), 5564. https://doi.org/10.1159/000323668Google Scholar
Derenzini, M. (2000). The AgNORs. Micron, 31, 117120. https://doi.org/10.1016/S0968-4328(99)00067-0Google Scholar
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. Developmental Cell, 30(2), 123136. https://doi.org/10.1016/j.devcel.2014.05.012Google Scholar
Durán, E., Ocaña, F. M., 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. Behavioural Brain Research, 214(2), 480487. https://doi.org/10.1016/j.bbr.2010.06.010Google Scholar
Durán, E., Ocaña, F. M., Gómez, A., Jiménez-Moya, F., Broglio, C., Rodríguez, F., & Salas, C. (2008). Telencephalon ablation impairs goldfish allocentric spatial learning in a “hole-board” task. Acta Neurobiologiae Experimentalis, 68(4), 519525. PMID: 19112476.Google Scholar
Eichenbaum, H. (2000). A cortical–hippocampal system for declarative memory. Nature Reviews Neuroscience, 1, 4150. https://doi.org/10.1038/35036213CrossRefGoogle ScholarPubMed
Eichenbaum, H. (2004). Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron, 44(1), 109120. https://doi.org/10.1016/j.neuron.2004.08.028Google Scholar
Eichenbaum, H. (2014). Time cells in the hippocampus: A new dimension for mapping memories. Nature Reviews Neuroscience, 15(11), 732744. https://doi.org/10.1038/nrn3827Google Scholar
Eichenbaum, H. (2017). The role of the hippocampus in navigation is memory. Journal of Neurophysiology, 117(4), 17851796. https://doi.org/10.1152/jn.00005.2017Google Scholar
Eichenbaum, H., & Cohen, N. J. (2001). From conditioning to conscious recollection: Memory systems of the brain. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780195178043.001.0001Google Scholar
Eichenbaum, H., Otto, T., & Cohen, N. J. (1994). Two functional components of the hippocampal memory system. Behavioral and Brain Sciences, 17(3), 449517. https://doi.org/10.1017/S0140525X00035391Google Scholar
Eichenbaum, H., Stewart, C., & Morris, R. G. M. (1990). Hippocampal representation in place learning. Journal of Neuroscience, 10(11), 35313542. https://doi.org/10.1523/jneurosci.10-11-03531.1990Google Scholar
Ekstrom, A. D., & Ranganath, C. (2018). Space, time, and episodic memory: The hippocampus is all over the cognitive map. Hippocampus, 28(9), 680687. https://doi.org/10.1002/hipo.22750Google Scholar
Fotowat, H., Lee, C., Jun, J. J., & Maler, L. (2019). Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation. eLife, 8, e44119. DOI: https://doi.org/10.7554/eLife.44119Google Scholar
Fremouw, T., Jackson-Smith, P., & Kesner, R. P. (1997). Impaired place learning and unimpaired cue learning in hippocampal- lesioned pigeons. Behavioral Neuroscience, 111(5), 963975. https://doi.org/10.1037/0735-7044.111.5.955Google Scholar
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. F1000Research, 3, 120. https://doi.org/10.12688/f1000research.5595.2Google Scholar
García-Moreno, L. M., Conejo, N. M., Pardo, H. G., Gómez, M., Martín, F. R., Alonso, M. J., & Arias, J. L. (2001). Hippocampal AgNOR activity after chronic alcohol consumption and alcohol deprivation in rats. Physiology and Behavior, 72, 115121. https://doi.org/10.1016/S0031-9384(00)00408-XGoogle Scholar
Gouteux, S., Thinus-Blanc, C., & Vauclair, J. (2001). Rhesus monkeys use geometric and nongeometric information during a reorientation task. Journal of Experimental Psychology: General, 130(3), 505519. https://doi.org/10.1037/0096-3445.130.3.505Google Scholar
Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004): Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron, 44, 581584. https://doi.org/10.1016/j.neuron.2004.11.003Google Scholar
Hartley, T., Lever, C., Burgess, N., & O’Keefe, J. (2014). Space in the brain: How the hippocampal formation supports spatial cognition. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1635), 20120510. https://doi.org/10.1098/rstb.2012.0510CrossRefGoogle ScholarPubMed
Harvey-Girard, E., Giassi, A. C., & Maler, L. (2012). The organization of the gymnotiform fish pallium in relation to learning and memory: IV. Expression of conserved transcription factors and implications for the evolution of dorsal telencephalon. Journal of Comparative Neurology, 520, 33953413. https://doi.org/10.1002/cne.23107Google Scholar
Hermer, L., & Spelke, S. (1994). A geometric process for spatial reorientation in young children. Nature, 370, 5759 https://doi.org/10.1038/370057a0CrossRefGoogle ScholarPubMed
Holding, M. L., Frazier, J. A., Taylor, E. N., & Strand, C. R. (2012) Experimentally altered navigational demands induce changes in the cortical forebrain of free-ranging Northern Pacific rattlesnakes (Crotalus o. oreganus). Brain, Behavior & Evolution, 79, 144154. https://doi.org/10.1159/000335034CrossRefGoogle ScholarPubMed
Ishikawa, Y., Yamamoto, N., Yoshimoto, M., Yasuda, T., Maruyama, K., Kage, T., Takeda, H., & Ito, H. (2007). Developmental origin of diencephalic sensory relay nuclei in teleosts. Brain, Behavior and Evolution, 69, 8795. https://doi.org/10.1159/000095197Google Scholar
Kamil, A. C., & Jones, J. E. (1997). The seed-storing corvid Clark’s nutcracker learns geometric relationships among landmarks. Nature, 390, 276279. https://doi.org/10.1038/36840Google Scholar
Kesner, R. P., & Rolls, E. T. (2015). A computational theory of hippocampal function, and tests of the theory: New developments. Neuroscience and Biobehavioral Reviews, 48, 92147. https://doi.org/10.1016/j.neubiorev.2014.11.009Google Scholar
Kim, J. J., & Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science, 256, 675677. https://doi.org/10.1126/science.1585183Google Scholar
Kitamura, T., Macdonald, C. J., & Tonegawa, S. (2015). Entorhinal–hippocampal neuronal circuits bridge temporally discontiguous events. Learning and Memory, 22, 438443. https://doi.org/10.1101/lm.038687.115Google Scholar
Leutgeb, S., & Leutgeb, J. K. (2007). Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learning and Memory, 14, 745757. https://doi.org/10.1101/lm.703907Google Scholar
López, J. C., Bingman, V. P., Rodríguez, F., Gómez, Y., & Salas, C. (2000). Dissociation of place and cue learning by telencephalic ablation in goldfish. Behavioral Neuroscience, 114, 687699. https://doi.org/10.1037/0735-7044.114.4.687Google Scholar
López, J. C., Broglio, C., Rodríguez, F., Thinus-Blanc, C., & Salas, C. (1999). Multiple spatial learning strategies in goldfish (Carassius auratus). Animal Cognition, 2, 109120. https://doi.org/10.1007/s100710050031Google Scholar
López, J. C., Gómez, Y., Vargas, J. P., & Salas, C. (2003). Spatial reversal learning deficit after medial cortex lesion in turtles. Neuroscience Letters, 341, 197200. https://doi.org/10.1016/S0304-3940(03)00186-1Google Scholar
López, J. C., Vargas, J. P., Gómez, Y., & Salas, C. (2003). Spatial and non-spatial learning in turtles: The role of medial cortex. Behavioural Brain Research, 143, 109120. https://doi.org/10.1016/S0166-4328(03)00030-5.Google Scholar
MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011). Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron, 71, 737749. https://doi.org/10.1016/j.neuron.2011.07.012Google Scholar
Maren, S., & Quirk, G. J. (2004). Neuronal signaling of fear memory. Nature Reviews Neuroscience, 5, 844852. https://doi.org/10.1038/nrn1535Google Scholar
Meck, W. H., Church, R. M., & Olton, D. S. (1984). Hippocampus, time, and memory. Behavioral Neuroscience, 98, 322. https://doi.org/10.1037/0735-7044.98.1.3Google Scholar
Moser, E. I., Kropff, E., & Moser, M.-B. (2008). Place cells, grid cells, and the brain’s spatial representation system. Annual Review of Neuroscience, 31, 6989. https://doi.org/10.1146/annurev.neuro.31.061307.090723CrossRefGoogle ScholarPubMed
Nelson, J. S., Grande, T. C., & Wilson, M. V. H. (2016). Fishes of the world. John Wiley & Sons. https://doi.org/10.1111/jfb.13229Google Scholar
Nieuwenhuys, R. (1963). The comparative anatomy of the actinopterygian forebrain. Journal für Hirnforschung, 6, 171192. PMID: 14121233.Google Scholar
Nieuwenhuys, R. (2011). The development and general morphology of the telencephalon of actinopterygian fishes: Synopsis, documentation and commentary. Brain Structure and Function, 215, 141157. https://doi.org/10.1007/s00429-010-0285-6Google Scholar
Northcutt, R. G. (2006). Connections of the lateral and medial divisions of the goldfish telencephalic pallium. Journal of Comparative Neurology, 494, 903943. https://doi.org/10.1002/cne.20853Google Scholar
Northcutt, R. G., & Braford, M. R. (1980). New observations on the organization and evolution of the telencephalon in actinopterygian fishes. In Ebbesson, S. O. E. (Ed.), Comparative neurology of the telencephalon (pp. 4198). Plenum Press. https://doi.org/10.1007/978-1-4613-2988-6_3Google Scholar
Ocaña, F. M., Uceda, S., Arias, J. L., Salas, C., & Rodríguez, F. (2017). Dynamics of goldfish subregional hippocampal pallium activity throughout spatial memory formation. Brain, Behavior and Evolution, 90(2), 154170. https://doi.org/10.1159/000478843Google Scholar
O’Keefe, J., & Nadel, L. (1978) The hippocampus as a cognitive map. Clarendon Press.Google Scholar
Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience, 106, 274285. https://doi.org/10.1037/0735-7044.106.2.274Google Scholar
Portavella, M., Torres, B., & Salas, C. (2004). Avoidance response in goldfish: Emotional and temporal involvement of medial and lateral telencephalic pallium. Journal of Neuroscience, 24, 23352342. https://doi.org/10.1523/JNEUROSCI.4930-03.2004Google Scholar
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. Animal Learning and Behavior, 22, 409420. https://doi.org/10.3758/BF03209160Google Scholar
Rodríguez, F., López, J. C., Vargas, J. P., Gómez, Y., Broglio, C., & Salas, C. (2002). Conservation of spatial memory function in the pallial forebrain of amniotes and ray-finned fishes. Journal of Neuroscience, 22, 28942903. https://doi.org/20026211Google Scholar
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. Neurobiology of Learning and Memory, 139, 128134. https://doi.org/10.1016/j.nlm.2017.01.002Google Scholar
Rolls, E. T. (2013). The mechanisms for pattern completion and pattern separation in the hippocampus. Frontiers in Systems Neuroscience, 7, 74. https://doi.org/10.3389/fnsys.2013.00074Google Scholar
Salas, C., Broglio, C., & Rodríguez, F. (2003). Evolution of forebrain and spatial cognition in vertebrates: Conservation across diversity. Brain, Behavior and Evolution, 62, 7282. https://doi.org/10.1159/000072438Google Scholar
Salas, C., Rodríguez, F., Vargas, J. P., Durán, E., & Torres, B. (1996). Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. Behavioral Neuroscience, 110, 965980. https://doi.org/10.1037/0735-7044.110.5.965Google Scholar
Schiller, D., Eichenbaum, H., Buffalo, E. A., Davachi, L., Foster, D. J., Leutgeb, S., & Ranganath, C. (2015). Memory and space: Towards an understanding of the cognitive map. Journal of Neuroscience, 35(41), 1390413911. https://doi.org/10.1523/JNEUROSCI.2618-15.2015Google Scholar
Schluessel, V., & Bleckmann, H. (2005). Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. Journal of Comparative Physiology, A191, 695706. https://doi.org/10.1007/s00359-005-0625-9Google Scholar
Sotelo, M. I., Daneri, M. F., Bingman, V. P., & Muzio, R. N. (2016). Telencephalic neuronal activation associated with spatial memory in the terrestrial toad Rhinella arenarum: Participation of the medial pallium during navigation by geometry. Brain, Behavior and Evolution, 88, 149160. https://doi.org/10.1159/000447441Google Scholar
Sovrano, V. A., Bisazza, A., & Vallortigara, G. (2003). Modularity as a fish (Xenotoca eiseni) views it: Conjoining geometric and nongeometric information for spatial reorientation. Journal of Experimental Psychology: Animal Behavior Processes, 29, 199210. https://doi.org/10.1037/0097-7403.29.3.199Google Scholar
Squire, L. R., Stark, C. E., & Clark, R. E. (2004) The medial temporal lobe. Annual Review of Neuroscience, 27, 279306. http://dx.doi.org/10.1146/annurev.neuro.27.070203.144130.Google Scholar
Staresina, B. P., & Davachi, L. (2009). Mind the gap: Binding experiences across space and time in the human hippocampus. Neuron, 63, 267276. https://doi.org/10.1016/j.neuron.2009.06.024.MindGoogle Scholar
Striedter, G. F., & Northcutt, R. G. (2020). Brains through time: A natural history of vertebrates. Oxford University Press. https://doi.org/10.1093/oso/9780195125689.001.0001Google Scholar
Thinus-Blanc, C. (1996). Animal spatial cognition: Behavioral and neural approaches. World Scientific Publishing. https://doi.org/10.1142/3246CrossRefGoogle Scholar
Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55, 189208. https://doi.org/10.1037/h0061626Google Scholar
Tommasi, L., Chiandetti, C., Pecchia, T., Sovrano, V. A., & Vallortigara, G. (2012). From natural geometry to spatial cognition. Neuroscience and Biobehavioral Reviews, 36, 799824. https://doi.org/10.1016/j.neubiorev.2011.12.007Google Scholar
Trinh, A. T., Clarke, S. E., Harvey-Girard, E., & Maler, L. (2019). Cellular and network mechanisms may generate sparse coding of sequential object encounters in hippocampal-like circuits. eNeuro, 6(4), 121. https://doi.org/10.1523/ENEURO.0108-19.2019.Google Scholar
Uceda, S., Ocaña, F. M., 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. Behavioural Brain Research, 292, 403408. https://doi.org/10.1016/j.bbr.2015.06.018Google Scholar
Vargas, J. P., López, J. C., Salas, C., & Thinus-Blanc, C. (2004). Encoding of geometric and featural spatial information by goldfish (Carassius auratus). Journal of Comparative Psychology, 118, 206216. https://doi.org/10.1037/0735-7036.118.2.206Google Scholar
Vargas, J. P., Rodríguez, F., López, J. C., Arias, J. L., & Salas, C. (2000). Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish. Brain Research, 865, 7784. https://doi.org/10.1016/S0006-8993(00)02220-4Google Scholar
Vinepinsky, E., Cohen, L., Perchik, S., Ben‑Shahar, O., Donchin, O., & Segev, R. (2020). Representation of edges, head direction, and swimming kinematics in the brain of freely‑navigating fish. Scientific Reports, 10, 14762. https://doi.org/10.1038/s41598-020-71217-1Google Scholar
Wong-Riley, M. T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience, 12, 94101. https://doi.org/10.1016/0166-2236(89)90165-3Google Scholar
Wullimann, M. F., & Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. Journal of Comparative Neurology, 75, 143162. https://doi.org/10.1002/cne.20183Google Scholar
Yamamoto, N., Ishikawa, Y., Yoshimoto, M., Xue, H. G., Bahaxar, N., Sawai, N., Yang, C. Y., Ozawa, H., & Ito, H. (2007). A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain, Behavior and Evolution, 69, 96104. https://doi.org/10.1159/000095198Google Scholar

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