Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish
Abstract
In mammals and birds different pallial forebrain areas participate in separate memory systems. In particular, the hippocampal pallium is implicated in spatial memory and temporal attribute processing, whereas the amygdalar pallium is involved in emotional memory. Here we analyze the involvement of teleost fish lateral and medial pallia, proposed as homologous to the hippocampus and amygdala, respectively, in a variety of learning and memory tasks, such as spatial memory; reversal learning; delay or trace motor classical conditioning; heart rate, emotional classical conditioning; and two way active avoidance conditioning. Results show that the damage to the lateral pallium produces a profound deficit in spatial learning and memory in teleost fish. In addition, lateral pallium lesions produce a significant deficit in trace classical conditioning, whereas they have no significant effects on delay conditioning, or in heart rate conditioning. In contrast, medial pallium lesions disrupt emotional, heart rate conditioning and avoidance conditioning, but spare spatial memory and temporal stimulus processing. These data demonstrate a striking functional similarity between the medial and lateral pallia of teleost fish and the pallial amygdala and hippocampal pallium of land vertebrates, respectively. The reviewed evidence suggest that these two separate memory systems, the hippocampus-dependent spatial, relational or temporal memory system, and the amygdala based emotional memory system, could have appeared early during evolution, having conserved their functional identity through vertebrate phylogenesis.
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Experimental studies using well-controlled behavioral procedures combined with brain lesion, neural activity recording, and neuro-morphofunctional techniques have provided evidence on the critical role of the teleost fish hippocampal pallium in spatial cognition.
“A growing number of experimental studies using well-controlled behavioral procedures combined with brain lesion, neural activity recording, and neuro-morphofunctional techniques have provided evidence on the critical role of the teleost fish hippocampal pallium in spatial cognition [28,112,157,180,181,182,183,184,185,186].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [180]
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
THE COMPARATIVE ANATOMY OF THE NERVOUS SYSTEM OF VERTEBRATES INCLUDING MAN
Ariëns, K. C. U., Huber, G. C., & Grosby, E. C. (1936) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-193611000-00044 · Cited by 2,096 · see citing works
EVOLUTION OF THE BRAIN AND INTELLIGENCE
Radinsky, L., & Jerison, H. J. (1975) · Evolution · doi:10.2307/2407154 · Cited by 1,982 · see citing works
PHYLOGENETICS: THE THEORY AND PRACTICE OF PHYLOGENETIC SYSTEMATICS
Fitch, W. M. (1982) · Evolution · doi:10.1111/j.1558-5646.1982.tb05453.x · Cited by 1,811 · see citing works
Vertebrate Paleontology and Evolution
Ostrom, J. H., & Carroll, R. L. (1988) · Palaios · doi:10.2307/3514548 · Cited by 1,677 · see citing works
The Central Nervous System of Vertebrates
Nieuwenhuys, R., ten Donkelaar, H. J., & Nicholson, C. (1998) · doi:10.1007/978-3-642-18262-4 · Cited by 1,249 · see citing works
Romer, A. S. (1971) · Andalas University Repository (Andalas University) · Cited by 981 · see citing works
Comparative vertebrate neuroanatomy: evolution and adaptation
(1996) · Choice Reviews Online · doi:10.5860/choice.34-0925 · Cited by 800 · see citing works
Solomon, P. R., Schaaf, E. R. V., Thompson, R. F., & Weisz, D. J. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.5.729 · Cited by 724 · see citing works
Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.5.729 · Cited by 724 · see citing works
Evolution of the Brain and Intelligence
(1973) · Elsevier eBooks · doi:10.1016/b978-0-123-85250-2.x5001-9 · Cited by 667 · see citing works
The Comparative Anatomy of the Nervous System of Vertebrates Including Man.
(1937) · Annals of Internal Medicine · doi:10.7326/0003-4819-11-1-226 · Cited by 509 · see citing works
Neurobiology of comparative cognition
Walker, S. F. (1991) · Biological Psychology · doi:10.1016/0301-0511(91)90020-h · Cited by 398 · see citing works
Kofoid, C. A. (1929) · American Journal of Public Health and the Nations Health · doi:10.2105/ajph.19.6.701-b · Cited by 333 · see citing works
Conservation of Spatial Memory Function in the Pallial Forebrain of Reptiles and Ray-Finned Fishes
Rodrı́guez, F., López, J. C., Vargas, J. P., Gómez, Y., Broglio, C., & Salas, C. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02894.2002 · Cited by 316 · see citing works
Self-citationSarter, M. F., & Markowitsch, H. J. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.2.342 · Cited by 294 · see citing works
Rodrı́guez, F., López, J. C., Vargas, J. P., Broglio, C., Gómez, Y., & Salas, C. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00682-7 · Cited by 293 · see citing works
Self-citationMemory systems in the brain and localization of a memory
Thompson, R. F., & Kim, J. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13438 · Cited by 291 · see citing works
Neurobiology of Comparative Cognition
(2014) · Psychology Press eBooks · doi:10.4324/9781315808147 · Cited by 287 · see citing works
Portavella, M., Torres, B., & Salas, C. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4930-03.2004 · Cited by 283 · see citing works
Self-citationThe Hippocampal and Parietal Foundations of Spatial Cognition
Burgess, N., Jeffery, K. J., & O'Keefe, J. M. (1999) · Cited by 249 · see citing works
The Forebrain of Gnathostomes: In Search of a Morphotype; pp. 275–288
Northcutt, R. G. (2008) · Brain, Behavior and Evolution · doi:10.1159/000113279 · Cited by 233 · see citing works
Comparative Aspects of Forebrain Organization in the Ray-Finned Fishes: Touchstones or Not?
Braford, M. R. (2008) · Brain Behavior and Evolution · doi:10.1159/000113278 · Cited by 202 · see citing works
Wullimann, M. F., & Rink, E. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00666-9 · Cited by 181 · see citing works
Evolution of forebrain and spatial cognition in vertebrates: Conservation across diversity
Salas, C., Broglio, C., & Rodríguez, F. (2003) · Brain, Behavior and Evolution · doi:10.1159/000072438 · Cited by 174 · see citing works
Self-citationGentile, C. G., Jarrell, T. W., Teich, A. H., McCabe, P. M., & Schneiderman, N. (1986) · Behavioural Brain Research · doi:10.1016/0166-4328(86)90226-3 · Cited by 153 · see citing works
Cognitive and emotional functions of the teleost fish cerebellum
Rodrı́guez, F., Durán, E., Gómez, A., Ocaña, F. M., Álvarez, E., Jiménez-Moya, F., Broglio, C., & Salas, C. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.026 · Cited by 148 · see citing works
Self-citationLee, T., & Kim, J. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5382-03.2004 · Cited by 146 · see citing works
Salas, C., Rodrı́guez, F., Vargas, J. P., Durán, E., & Torres, B. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.5.965 · Cited by 142 · see citing works
Self-citationDissociation of place and cue learning by telencephalic ablation in goldfish.
López, J. C., Bingman, V. P., Rodríguez, F., Gómez, Y., & Salas, C. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.4.687 · Cited by 93 · see citing works
Self-citationLópez, J. C., Broglio, C., Rodrı́guez, F., Thinus‐Blanc, C., & Salas, C. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00167-9 · Cited by 91 · see citing works
Self-citationPortavella, M., Torres, B., Salas, C., & Papini, M. R. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.01.083 · Cited by 90 · see citing works
Self-citationVargas, J. P., Rodrı́guez, F., López, J. C., Arias, J. L., & Salas, C. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02220-4 · Cited by 88 · see citing works
Self-citationGormezano, I. (2013) · Psychology Press eBooks · doi:10.4324/9780203772515 · Cited by 86 · see citing works
Comparative correlative neuroanatomy of the vertebrate telencephalon
(1984) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(84)90187-1 · Cited by 55 · see citing works
Brain substrates of “eyeblink” classical conditioning in goldfish
Álvarez, E., Gómez, A., Durán, E., Ocaña, F. M., Jiménez-Moya, F., Broglio, C., Rodrı́guez, F., & Salas, C. (2003) · Acta Neurobiologiae Experimentalis · Cited by 10 · see citing works
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Grandel, H., Kaslin, J., Ganz, J., Wenzel, I., & Brand, M. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.040 · Cited by 553 · see citing works
Neurogenesis in zebrafish – from embryo to adult
Viales, R. R., Strähle, U., & Scholpp, S. (2013) · Neural Development · doi:10.1186/1749-8104-8-3 · Cited by 374 · see citing works
Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain
Kaslin, J., Ganz, J., & Brand, M. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.2015 · Cited by 354 · see citing works
The evolution of episodic memory
Allen, T. A., & Fortin, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301199110 · Cited by 350 · see citing works
Key, B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1011 · Cited by 318 · see citing works
Resynthesizing behavior through phylogenetic refinement
Cisek, P. (2019) · Attention Perception & Psychophysics · doi:10.3758/s13414-019-01760-1 · Cited by 294 · see citing works
März, M., Chapouton, P., Diotel, N., Vaillant, C., Hesl, B., Takamiya, M., Lam, C. S., Kah, O., Bally‐Cuif, L., & Strähle, U. (2010) · Glia · doi:10.1002/glia.20971 · Cited by 257 · see citing works
Parimisetty, A., Dorsemans, A.-C., Awada, R., Ravanan, P., Diotel, N., & d’Hellencourt, C. L. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0530-x · Cited by 208 · see citing works
Neuropsychology of Learning and Memory in Teleost Fish
Salas, C., Broglio, C., Durán, E., Gómez, A., Ocaña, F. M., Jiménez-Moya, F., & Rodríguez, F. (2006) · Zebrafish · doi:10.1089/zeb.2006.3.157 · Cited by 189 · see citing works
Self-citationEnvironmental effects on fish neural plasticity and cognition
Ebbesson, L. O. E., & Braithwaite, V. A. (2012) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2012.03486.x · Cited by 185 · see citing works
Burns, J. G., & Rodd, F. H. (2008) · Animal Behaviour · doi:10.1016/j.anbehav.2008.02.017 · Cited by 180 · see citing works
Moreno, N., & González, A. (2007) · Journal of Anatomy · doi:10.1111/j.1469-7580.2007.00780.x · Cited by 164 · see citing works
Pain perception, aversion and fear in fish
Braithwaite, V. A., & Boulcott, P. (2007) · Diseases of Aquatic Organisms · doi:10.3354/dao075131 · Cited by 148 · see citing works
Cognitive and emotional functions of the teleost fish cerebellum
Rodrı́guez, F., Durán, E., Gómez, A., Ocaña, F. M., Álvarez, E., Jiménez-Moya, F., Broglio, C., & Salas, C. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.026 · Cited by 148 · see citing works
Self-citationHeterogeneity and Fgf dependence of adult neural progenitors in the zebrafish telencephalon
Ganz, J., Kaslin, J., Hochmann, S., Freudenreich, D., & Brand, M. (2010) · Glia · doi:10.1002/glia.21012 · Cited by 138 · see citing works
Subdivisions of the adult zebrafish pallium based on molecular marker analysis
Ganz, J., Kroehne, V., Freudenreich, D., Machate, A., Geffarth, M., Braasch, I., Kaslin, J., & Brand, M. (2014) · F1000Research · doi:10.12688/f1000research.5595.1 · Cited by 156 · see citing works
Hinsch, K., & Zupanc, G. K. H. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.01.071 · Cited by 130 · see citing works
Mellor, D. J. (2019) · Animals · doi:10.3390/ani9070440 · Cited by 139 · see citing works
Alderman, S. L., & Bernier, N. J. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21332 · Cited by 115 · see citing works
Selective involvement of the goldfish lateral pallium in spatial memory
Broglio, C., Rodríguez, F., Gómez, A., Arias, J. L., & Salas, C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.031 · Cited by 112 · see citing works
Self-citationCold-Blooded Cognition: Reptilian Cognitive Abilities
Wilkinson, A., & Huber, L. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199738182.013.0008 · Cited by 111 · see citing works
Secondary neurogenesis and telencephalic organization in zebrafish and mice: a brief review
Wullimann, M. F. (2009) · Integrative Zoology · doi:10.1111/j.1749-4877.2008.00140.x · Cited by 100 · see citing works
Distribution of cannabinoid receptor 1 in the CNS of zebrafish
Lam, C. S., Rastegar, S., & Strähle, U. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.069 · Cited by 99 · see citing works
Teles, M. C., Cardoso, S. D., & Oliveira, R. F. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00016 · Cited by 96 · see citing works
Durán, E., Ocaña, F. M., Broglio, C., Rodríguez, F., & Salas, C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.06.010 · Cited by 90 · see citing works
Self-citationDiotel, N., Lübke, L., Strähle, U., & Rastegar, S. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.568930 · Cited by 93 · see citing works
The cellular composition of neurogenic periventricular zones in the adult zebrafish forebrain
Lindsey, B. W., Darabie, A. A., & Tropepe, V. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23065 · Cited by 88 · see citing works
Learning in cod (Gadus morhua): long trace interval retention
Nilsson, J., Kristiansen, T., Fosseidengen, J. E., Fernö, A., & van den Bos, R. (2007) · Animal Cognition · doi:10.1007/s10071-007-0103-6 · Cited by 81 · see citing works
Resistin: A journey from metabolism to cancer
Deb, A., Deshmukh, B., Ramteke, P. L., Bhati, F. K., & Bhat, M. K. (2021) · Translational Oncology · doi:10.1016/j.tranon.2021.101178 · Cited by 84 · see citing works
Zebrafish reward mutants reveal novel transcripts mediating the behavioral effects of amphetamine
Webb, K. J., Norton, W., Trümbach, D., Meijer, A. H., Ninkovic, J., Topp, S., Heck, D., Marr, C., Wurst, W., Theis, F. J., et al. (2009) · Genome biology · doi:10.1186/gb-2009-10-7-r81 · Cited by 81 · see citing works
Personality Traits and Behaviour
Budaev, S. V., & Brown, C. (2011) · doi:10.1002/9781444342536.ch7 · Cited by 78 · see citing works
Variation in Emotion and Cognition Among Fishes
Braithwaite, V. A., Huntingford, F. A., & van den Bos, R. (2011) · Journal of Agricultural and Environmental Ethics · doi:10.1007/s10806-011-9355-x · Cited by 76 · see citing works
González‐Voyer, A., Winberg, S., & Kolm, N. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-238 · Cited by 75 · see citing works
“Limbic associative” and “autonomic” amygdala in teleosts: A review of the evidence
Maximino, C., Lima, M. G., Oliveira, K. R. M., Batista, E. D. J. O., & Herculano, A. M. (2012) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2012.10.001 · Cited by 72 · see citing works
Impact of noise on development, physiological stress and behavioural patterns in larval zebrafish
Lara, R. A., & Vasconcelos, R. O. (2021) · Scientific Reports · doi:10.1038/s41598-021-85296-1 · Cited by 72 · see citing works
Manuel, R., Gorissen, M., Zethof, J., Ebbesson, L. O. E., van de Vis, H., Flik, G., & van den Bos, R. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.109736 · Cited by 69 · see citing works
Manuel, R., Gorissen, M., Stokkermans, M., Zethof, J., Ebbesson, L. O. E., van de Vis, H., Flik, G., & van den Bos, R. (2015) · Zebrafish · doi:10.1089/zeb.2014.1045 · Cited by 68 · see citing works
The neuroecology of the water-to-land transition and the evolution of the vertebrate brain
MacIver, M. A., & Finlay, B. L. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0523 · Cited by 70 · see citing works
Lindsey, B. W., & Tropepe, V. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22183 · Cited by 66 · see citing works
Neural systems that facilitate the representation of social rank
Dwortz, M. F., Curley, J. P., Tye, K. M., & Padilla-Coreano, N. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0444 · Cited by 64 · see citing works
Giassi, A. C. C., Duarte, T. T., Ellis, W., & Maler, L. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23109 · Cited by 61 · see citing works
Social plasticity in fish: integrating mechanisms and function
Oliveira, R. F. (2012) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2012.03477.x · Cited by 61 · see citing works
Elliott, S. B., Harvey‐Girard, E., Giassi, A. C. C., & Maler, L. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24060 · Cited by 61 · see citing works
Lindsey, B. W., Hall, Z. J., Heuzé, A., Joly, J., Tropepe, V., & Kaslin, J. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.06.004 · Cited by 60 · see citing works
Subdivisions of the adult zebrafish pallium based on molecular marker analysis
Ganz, J., Kroehne, V., Freudenreich, D., Machate, A., Geffarth, M., Braasch, I., Kaslin, J., & Brand, M. (2015) · F1000Research · doi:10.12688/f1000research.5595.2 · Cited by 60 · see citing works
Manuel, R., Gorissen, M., Pizà‐Roca, C., Zethof, J., van de Vis, H., Flik, G., & van den Bos, R. (2014) · Zebrafish · doi:10.1089/zeb.2013.0970 · Cited by 60 · see citing works
Spatial Cognition in Teleost Fish: Strategies and Mechanisms
Rodríguez, F., Quintero, B., Amores, L., Madrid, D., Salas-Peña, C., & Salas, C. (2021) · Animals · doi:10.3390/ani11082271 · Cited by 59 · see citing works
Self-citationEnvironmental enrichment as an experience-dependent modulator of social plasticity and cognition
Gubert, C., & Hannan, A. J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.03.033 · Cited by 59 · see citing works
Diotel, N., Viales, R. R., Armant, O., März, M., Ferg, M., Rastegar, S., & Strähle, U. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23733 · Cited by 58 · see citing works
Proliferation zones in adult medaka (Oryzias latipes) brain
Kuroyanagi, Y., Okuyama, T., Suehiro, Y., Imada, H., Shimada, A., Naruse, K., Takeda, H., Kubo, T., & Takeuchi, H. (2010) · Brain Research · doi:10.1016/j.brainres.2010.01.045 · Cited by 54 · see citing works
Cross-modal object recognition and dynamic weighting of sensory inputs in a fish
Schumacher, S., de Perera, T. B., Thenert, J., & von der Emde, G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603120113 · Cited by 53 · see citing works
Isolation impairs cognition in a social fish
Brandão, M. L., Braithwaite, V. A., & Gonçalves‐de‐Freitas, E. (2015) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2015.08.026 · Cited by 51 · see citing works
Dorsomedial pallium lesions impair taste aversion learning in goldfish
Martín-Monzón, I., Gómez, A., Salas, C., Puerto, A., & Rodrı́guez, F. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.06.003 · Cited by 51 · see citing works
Self-citationProkineticin 2 Expression Is Associated with Neural Repair of Injured Adult Zebrafish Telencephalon
Ayari, B., Hachimi, K. H. E., Yanicostas, C., Landoulsi, A., & Soussi‐Yanicostas, N. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.0972 · Cited by 51 · see citing works
Behavioral Evidence of Felt Emotions
Weary, D. M., Droege, P., & Braithwaite, V. A. (2017) · Advances in the study of behavior · doi:10.1016/bs.asb.2017.02.002 · Cited by 50 · see citing works
Cerqueira, M. A. C., Millot, S., Félix, A. S., Silva, T. S., Oliveira, G. A., Oliveira, C. C. V., Rey, S., MacKenzie, S. A., & Oliveira, R. F. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.2922 · Cited by 49 · see citing works
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Zacks, O., & Jablonka, E. (2023) · Neuroscience of Consciousness · doi:10.1093/nc/niad020 · Cited by 47 · see citing works
Varga, Z. K., Zsigmond, Á., Pejtsik, D., Varga, M., Demeter, K., Mikics, É., Haller, J., & Aliczki, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-34989-1 · Cited by 46 · see citing works
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Nilsson, J., Kristiansen, T., Fosseidengen, J. E., Fernö, A., & van den Bos, R. (2008) · Animal Cognition · doi:10.1007/s10071-008-0155-2 · Cited by 45 · see citing works
Brain and Cognition in Teleost Fish
Broglio, C., Gómez, A., Durán, E., Salas, C., & Rodrı́guez, F. (2011) · Wiley eBooks · doi:10.1002/9781444342536.ch15 · Cited by 44 · see citing works
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Krug, R. G., & Clark, K. J. (2015) · Gene · doi:10.1016/j.gene.2015.07.036 · Cited by 44 · see citing works
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Mes, D., Palstra, A. P., Henkel, C. V., Mayer, I., & Vindas, M. A. (2020) · Royal Society Open Science · doi:10.1098/rsos.191640 · Cited by 45 · see citing works
Fernández‐Teruel, A., & Tobeña, A. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.08.014 · Cited by 43 · see citing works
Karoubi, N., Segev, R., & Wullimann, M. F. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00106 · Cited by 43 · see citing works
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Rodrı́guez, F., Broglio, C., Durán, E., Gómez, A., & Salas, C. (2006) · Wiley eBooks · doi:10.1002/9780470996058.ch13 · Cited by 42 · see citing works
Self-citationGiassi, A. C. C., Harvey‐Girard, E., Valsamis, B., & Maler, L. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23097 · Cited by 41 · see citing works
Cummings, M. E. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.02.021 · Cited by 41 · see citing works
Neindre, P. L., Bernard, É., Boissy, A., Boivin, X., Calandreau, L., Delon, N., Deputte, B. L., Desmoulin‐Canselier, S., Dunier, M., Faivre, N., et al. (2017) · EFSA Supporting Publications · doi:10.2903/sp.efsa.2017.en-1196 · Cited by 42 · see citing works
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Pinheiro‐da‐Silva, J., Tran, S., & Luchiari, A. C. (2018) · Behavioural Processes · doi:10.1016/j.beproc.2018.04.004 · Cited by 39 · see citing works
Cerebellum lesion impairs eyeblink-like classical conditioning in goldfish
Gómez, A., Durán, E., Salas, C., & Rodrı́guez, F. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.12.018 · Cited by 39 · see citing works
Self-citationSchluessel, V., Kraniotakes, H., & Bleckmann, H. (2013) · Animal Cognition · doi:10.1007/s10071-013-0667-2 · Cited by 38 · see citing works
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Ruhl, T., Prinz, N., Oellers, N., Seidel, N. I., Jonas, A., Albayram, Ö., Bilkei‐Gorzó, A., & von der Emde, G. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3522-5 · Cited by 37 · see citing works
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Ampatzis, K., & Dermon, C. R. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22278 · Cited by 37 · see citing works
Papoutsoglou, S. E., Karakatsouli, N., Batzina, A., Papoutsoglou, E. S., & Tsopelakos, A. (2008) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2008.02001.x · Cited by 37 · see citing works
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Fuss, T., Bleckmann, H., & Schluessel, V. (2014) · Journal of Comparative Physiology A · doi:10.1007/s00359-013-0859-x · Cited by 34 · see citing works
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Imperatore, R., D’Angelo, L., Safari, O., Motlagh, H. A., Piscitelli, F., de Girolamo, P., Cristino, L., Varricchio, E., Marzo, V. D., & Paolucci, M. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00062 · Cited by 31 · see citing works
Cacialli, P., D’Angelo, L., Kah, O., Coumailleau, P., Guéguen, M., Pellegrini, E., & Lucini, C. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24352 · Cited by 30 · see citing works
Fong, S., Rogell, B., Amcoff, M., Kotrschal, A., van der Bijl, W., Buechel, S. D., & Kolm, N. (2021) · Science Advances · doi:10.1126/sciadv.abj4314 · Cited by 30 · see citing works
Urzainqui, I. Q., Rodríguez‐Moldes, I., Mazan, S., & Candal, E. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0834-5 · Cited by 30 · see citing works
Manns, J. R., & Eichenbaum, H. (2007) · Evolution of Nervous Systems · doi:10.1016/b0-12-370878-8/00086-0 · Cited by 28 · see citing works
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Nilsson, J., Stien, L. H., Fosseidengen, J. E., Olsen, R. E., & Kristiansen, T. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.02.014 · Cited by 26 · see citing works
Thomson, J. S., Deakin, A. G., Cossins, A. R., Spencer, J. W., Young, I. S., & Sneddon, L. U. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.224527 · Cited by 25 · see citing works
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Self-citationFuss, T., Bleckmann, H., & Schluessel, V. (2014) · Journal of Comparative Physiology A · doi:10.1007/s00359-013-0858-y · Cited by 25 · see citing works
Podlasz, P., Jakimiuk, A., Kasica, N., Czaja, K., & Wa̧sowicz, K. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00239 · Cited by 23 · see citing works
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Uglem, I., Kristiansen, T., Mejdell, C. M., Basic, D., & Mortensen, S. (2019) · Reviews in Aquaculture · doi:10.1111/raq.12342 · Cited by 21 · see citing works
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Self-citation
- Authors
- Broglio, C., Gómez, A., Durán, E., Ocaña, F. M., Jiménez-Moya, F., Rodríguez, F., & Salas, C.
- Affiliations
- Universidad de Sevilla (ES)
- Corresponding author
- Broglio, C.
- Venue
- Brain Research Bulletin
- Publisher
- Elsevier BV
- Published
- 2005-09
- Volume
- 66
- Issue
- 4-6
- Pages
- 277-281
- ISSN
- 0361-9230 (ISSN-L)
- OpenAlex
- W2010578513
- Cited by
- 203
- References
- 37
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 8 · 2023: 6 · 2022: 9 · 2021: 10 · 2020: 11 · 2019: 10 · 2018: 8 · 2017: 10 · 2016: 12 · 2015: 14 · 2014: 13 · 2013: 9 · 2012: 13
- FWCI
- 4.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish biology, ecology, and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- pallium, medial pallium, spatial memory, emotional memory, temporal memory, classical conditioning, heart rate conditioning, avoidance conditioning, reversal learning, actinopterygian fishes, teleost evolution, forebrain evolution
- MeSH terms
- Animals, Avoidance Learning, Conditioning, Classical, Emotions, Fishes, Hippocampus, Memory, Space Perception
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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