Neuropsychology of learning and memory in teleost fish.

Traditionally, brain and behavior evolution was viewed as an anagenetic process that occurred in successive stages of increasing complexity and advancement. Fishes, considered the most primitive vertebrates, were supposed to have a scarcely differentiated telencephalon, and limited learning capabilities. However, recent developmental, neuroanatomical, and functional data indicate that the evolution of brain and behavior may have been more conservative than previously thought. Experimental data suggest that the properties and neural basis of learning and memory are notably similar among teleost fish and land vertebrates. For example, lesion studies show that the teleost cerebellum is essential in classical conditioning of discrete motor responses. The lateral telencephalic pallium of the teleost fish, proposed as homologous to the hippocampus, is selectively involved in spatial learning and memory, and in trace classical conditioning. In contrast, the medial pallium, considered homologous to the amygdala, is involved in emotional conditioning in teleost fish. The data reviewed here show a remarkable parallelism between mammals and teleost fish concerning the role of different brain centers in learning and memory and cognitive processes. These evidences suggest that these separate memory systems could have appeared early during the evolution of vertebrates, having been conserved through phylogenesis.

[1]  R. Nieuwenhuys,et al.  New etho-physiological experiments with male Gasterosteus aculeatus, with anatomical comment , 1963 .

[2]  W. Boshoven,et al.  Comparison of the amnestic effects of NMDA receptor antagonist MK-801 and nitric oxide synthase inhibitors: L-NAME and L-NOARG in goldfish. , 1998, Behavioral neuroscience.

[3]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[4]  G. Savage Some preliminary observations on the role of the telencephalon in food-reinforced behaviour in the goldgish, Carassius auratus. , 1969, Animal behaviour.

[5]  D. Sparks The brainstem control of saccadic eye movements , 2002, Nature Reviews Neuroscience.

[6]  L. Nadel The hippocampus and space revisited , 1991, Hippocampus.

[7]  M. Botez,et al.  Navigational deficits in weaver mutant mice , 1986, Brain Research.

[8]  Juan Pedro Vargas,et al.  Encoding of geometric and featural spatial information by goldfish (Carassius auratus). , 2004, Journal of comparative psychology.

[9]  Cristina Broglio,et al.  Conservation of Spatial Memory Function in the Pallial Forebrain of Reptiles and Ray-Finned Fishes , 2002, The Journal of Neuroscience.

[10]  J. D. Bruin Telencephalon and Behavior in Teleost Fish , 1980 .

[11]  D. M. Guthrie,et al.  Motor responses to localized electrical stimulation of the tectum in the freshwater perch (perca fluviatilis) , 1986, Neuroscience.

[12]  F. Rodríguez,et al.  Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish , 2002, Brain Research Bulletin.

[13]  M. Molinari,et al.  The cerebellum in the spatial problem solving: a co-star or a guest star? , 1998, Progress in Neurobiology.

[14]  R. N. Leaton,et al.  Cerebellar vermis: essential for classically conditioned bradycardia in the rat , 1990, Brain Research.

[15]  C. Bucherelli,et al.  Effects of nucleus basolateralis amygdalae neurotoxic lesions on aversive conditioning in the rat , 1991, Physiology & Behavior.

[16]  M. Braford,et al.  Comparative aspects of forebrain organization in the ray-finned fishes: touchstones or not? , 1995, Brain, behavior and evolution.

[17]  N. Kotchabhakdi Functional circuitry of the goldfish cerebellum , 2004, Journal of comparative physiology.

[18]  B Ghelarducci,et al.  Contribution of the cerebellar vermis to cardiovascular control. , 1996, Journal of the autonomic nervous system.

[19]  Benedetto Sacchetti,et al.  Cerebellar role in fear-conditioning consolidation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Abbate Recent papers on zebrafish and other aquarium fish models. , 2006, Zebrafish.

[21]  C. S. S.,et al.  The Comparative Anatomy of the Nervous System of Vertebrates, including Man , 1937, Nature.

[22]  W. Nolte Experimentelle Untersuchungen zum Problem der Lokalisation des Assoziationsvermögens im Fischgehirn , 1932, Zeitschrift für vergleichende Physiologie.

[23]  B. Torres,et al.  9 – On the Role of Goldfish Optic Tectum in the Generation of Eye Movements , 1994 .

[24]  Cristina Broglio,et al.  Evolution of Forebrain and Spatial Cognition in Vertebrates: Conservation across Diversity , 2003, Brain, Behavior and Evolution.

[25]  M. Papini,et al.  Involvement of the telencephalon in spaced-trial avoidance learning in the goldfish (Carassius auratus) , 2003, Physiology & Behavior.

[26]  R. Nieuwenhuys,et al.  The Central Nervous System of Vertebrates , 1997, Springer Berlin Heidelberg.

[27]  K. Uematsu,et al.  Involvement of the cerebellum in classical fear conditioning in goldfish , 2004, Behavioural Brain Research.

[28]  G. Savage The Fish Telencephalon and Its Relation to Learning , 1980 .

[29]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[30]  R. Nieuwenhuys,et al.  The Telencephalon of Actinopterygian Fishes , 1990 .

[31]  R. Davis,et al.  NMDA receptor antagonist MK-801 blocks learning of conditioned stimulus-unconditioned stimulus contiguity but not fear of conditioned stimulus in goldfish (Carassius auratus L.). , 1994, Behavioral neuroscience.

[32]  F. Rodríguez,et al.  Cognitive and emotional functions of the teleost fish cerebellum , 2005, Brain Research Bulletin.

[33]  R. Nieuwenhuys THE COMPARATIVE ANATOMY OF THE ACTINOPTERYGIAN FOREBRAIN. , 1963, Journal fur Hirnforschung.

[34]  G. Savage Behavioural effects of electrical stimulation of the telencephalon of the goldfish, Carassius auratus. , 1971, Animal behaviour.

[35]  J. Caston,et al.  Effects of early midline cerebellar lesion on cognitive and emotional functions in the rat , 2000, Behavioural Brain Research.

[36]  R. F. Thompson,et al.  Cerebellum: essential involvement in the classically conditioned eyelid response. , 1984, Science.

[37]  J. Overmier,et al.  4 – The Function of the Teleost Telencephalon in Behavior: A Reinforcement Mediator , 1978 .

[38]  Khashayar Farsad,et al.  Comparative Vertebrate Neuroanatomy: Evolution and Adaptation , 1996, The Yale Journal of Biology and Medicine.

[39]  M. Woodruff,et al.  Fornix lesions, plasma ACTH levels, and shuttle box avoidance in rats. , 1983, Behavioral neuroscience.

[40]  F. M. Ocaña,et al.  Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish , 2005, Brain Research Bulletin.

[41]  Juan P. Vargas,et al.  Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes , 1994 .

[42]  A. Riolobos Differential effect of chemical lesion and electrocoagulation of the central amygdaloid nucleus on active avoidance responses , 1986, Physiology & Behavior.

[43]  M. Schachner,et al.  Inhibition of memory consolidation by antibodies against cell adhesion molecules after active avoidance conditioning in zebrafish. , 1999, Journal of neurobiology.

[44]  E FRAUCHIGER,et al.  [COMPARATIVE NEUROLOGY]. , 1895, Der Nervenarzt.

[45]  Sherry,et al.  Behavioural and neural bases of orientation in food-storing birds , 1996, The Journal of experimental biology.

[46]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[47]  M. Fanselow,et al.  N-methyl-D-aspartate receptor antagonist APV blocks acquisition but not expression of fear conditioning. , 1991, Behavioral neuroscience.

[48]  B. Torres,et al.  Tectal codification of eye movements in goldfish studied by electrical microstimulation , 1997, Neuroscience.

[49]  J. Arias,et al.  Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish , 2000, Brain Research.

[50]  Catherine Thinus-Blanc,et al.  Reversal learning deficit in a spatial task but not in a cued one after telencephalic ablation in goldfish , 2000, Behavioural Brain Research.

[51]  R. N. Leaton,et al.  Lesions of the cerebellar vermis and cerebellar hemispheres: effects on heart rate conditioning in rats. , 1990, Behavioral neuroscience.

[52]  J. Disterhoft,et al.  Hippocampectomy disrupts trace eye-blink conditioning in rabbits. , 1990, Behavioral neuroscience.

[53]  C. Thinus-Blanc,et al.  Multiple spatial learning strategies in goldfish (Carassius auratus) , 1999, Animal Cognition.

[54]  B. Torres,et al.  Avoidance Response in Goldfish: Emotional and Temporal Involvement of Medial and Lateral Telencephalic Pallium , 2004, The Journal of Neuroscience.

[55]  Joseph E LeDoux Emotion: clues from the brain. , 1995, Annual review of psychology.

[56]  Michael Davis,et al.  Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala , 1990, Nature.

[57]  Xiaojuan Xu,et al.  NMDA receptor antagonist AP5 and nitric oxide synthase inhibitor 7-NI affect different phases of learning and memory in goldfish , 2001, Brain Research.

[58]  I. Duncan,et al.  Investigating Fear in Rainbow Trout (Oncorhynchus mykiss) Using the Conditioned-Suppression Paradigm , 2008, Journal of applied animal welfare science : JAAWS.

[59]  B W Agranoff,et al.  Actinomycin D Blocks Formation of Memory of Shock-Avoidance in Goldfish , 1967, Science.

[60]  V P Bingman,et al.  Dissociation of place and cue learning by telencephalic ablation in goldfish. , 2000, Behavioral neuroscience.

[61]  W. Turski,et al.  Excitatory amino acid antagonists and memory: Effect of drugs acting at N-methyl-d-aspartate receptors in learning and memory tasks , 1990, Neuropharmacology.

[62]  J. D. Bruin,et al.  Neural Correlates of Motivated Behavior in Fish , 1983 .

[63]  K. Jeffery,et al.  The Hippocampal and Parietal Foundations of Spatial Cognition , 1999 .

[64]  J J Kim,et al.  Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. , 1995, Behavioral neuroscience.

[65]  T. Teyler,et al.  Long-term potentiation in the goldfish optic tectum , 1986, Brain Research.

[66]  W. Boshoven,et al.  Comparison of the amnestic effects of NMDA receptor antagonist MK-801 and nitric oxide synthase inhibitors : L-NAME and L-NOARG in goldfish , 1998 .

[67]  R. Northcutt The forebrain of gnathostomes: in search of a morphotype. , 1995, Brain, behavior and evolution.

[68]  F. Rodríguez,et al.  Spatial cognition and its neural basis in teleost fishes , 2003 .

[69]  David A. Bengtson,et al.  Growth, survival and size-selective predation mortality of larval and juvenile inland silversides, Menidia beryllina (Pisces; Atherinidae) , 1996 .

[70]  Y. Dudai,et al.  Stability of Retrieved Memory: Inverse Correlation with Trace Dominance , 2003, Science.

[71]  B. Torres,et al.  Eye-movement recording in freely moving animals , 2001, Physiology & Behavior.

[72]  Stanley Fahn,et al.  Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon , 1983, Neurology.

[73]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[74]  Etsuro Ito,et al.  Long-term potentiation in the optic tectum of rainbow trout , 2004, Neuroscience Letters.

[75]  P. Laming,et al.  Cardiac, ventilatory and behavioural arousal responses evoked by electrical brain stimulation in the goldfish (Carassitis auratus) , 1988, Physiology & Behavior.

[76]  R. Fernald,et al.  How do social dominance and social information influence reproduction and the brain? , 2008, Integrative and comparative biology.

[77]  Sven O. E. Ebbesson,et al.  Comparative Neurology of the Telencephalon , 2011, Springer US.

[78]  WF Supple,et al.  The anterior cerebellar vermis: essential involvement in classically conditioned bradycardia in the rabbit , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Higher brain areas and functions , 1983 .

[80]  C. Kappers,et al.  The comparative anatomy of the nervous system of vertebrates, including man , 1936 .

[81]  Valeria Anna Sovrano,et al.  Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish , 2002, Cognition.

[82]  M. Wullimann,et al.  The teleostean forebrain: a comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization , 2002, Brain Research Bulletin.

[83]  Xiaojuan Xu,et al.  The role of telencephalic NMDA receptors in avoidance learning in goldfish (Carassius auratus). , 2003, Behavioral neuroscience.

[84]  C. Goodlett,et al.  Constraints on water maze spatial learning in rats Implications for behavioral studies of brain damage and recovery of function , 1988, Behavioural Brain Research.

[85]  B. Torres,et al.  Visual orienting response in goldfish: a multidisciplinary study , 2005, Brain Research Bulletin.

[86]  A. Butler Topography and topology of the teleost telencephalon: a paradox resolved , 2000, Neuroscience Letters.

[87]  Juan Carlos López,et al.  Telencephalic ablation in goldfish impairs performance in a ‘spatial constancy’ problem but not in a cued one , 1996, Behavioural Brain Research.

[88]  Tadashi Isa,et al.  Brainstem control of head movements during orienting; organization of the premotor circuits , 2002, Progress in Neurobiology.

[89]  J. Henley,et al.  Quantitative analysis of the distributions of glutamatergic ligand binding sites in goldfish brain , 1994, Brain Research.

[90]  R. Northcutt,et al.  New Observations on the Organization and Evolution of the Telencephalon of Actinopterygian Fishes , 1980 .

[91]  V P Bingman,et al.  The importance of comparative studies and ecological validity for understanding hippocampal structure and cognitive function , 1992, Hippocampus.

[92]  J. Delgado-García,et al.  Information processing underlying gaze control , 1994 .

[93]  Robert Lalonde,et al.  The cerebellum and learning processes in animals , 1990, Brain Research Reviews.

[94]  R. Nieuwenhuys,et al.  Holosteans and Teleosts , 1998 .

[95]  Sidney S. Simon,et al.  Merging of the Senses , 2008, Front. Neurosci..

[96]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[97]  Chang-Joong Lee,et al.  NMDA receptor-dependent long-term potentiation in the telencephalon of the zebrafish , 2004, Neuroscience Letters.

[98]  C Salas,et al.  Spatial and non-spatial learning in turtles: the role of medial cortex , 2003, Behavioural Brain Research.

[99]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[100]  C Salas,et al.  Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. , 1996, Behavioral neuroscience.

[101]  V. Bingman,et al.  Neuroethology of Avian Navigation , 1998 .

[102]  B. Torres,et al.  Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish , 1998, Experimental Brain Research.

[103]  B. Torres,et al.  Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus) , 2004, Neuroscience Letters.

[104]  E. B. Hale Social Facilitation and Forebrain Function in Maze Performance of Green Sunfish, Lepomis cyanellus , 1956, Physiological Zoology.

[105]  A. Dickinson,et al.  Episodic-like memory during cache recovery by scrub jays , 1998, Nature.

[106]  C. Salas,et al.  Spatial reversal learning deficit after medial cortex lesion in turtles , 2003, Neuroscience Letters.

[107]  B. Torres,et al.  Neural substrata underlying tectal eye movement codification in goldfish , 2002, Brain Research Bulletin.

[108]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[109]  E. Wiley Phylogenetics: The Theory and Practice of Phylogenetic Systematics , 1981 .

[110]  Haruko Matsui,et al.  Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behaviour , 1998, Nature.

[111]  J. McKENDRICK,et al.  The Central Nervous System of Vertebrates , 1909, Nature.

[112]  R. F. Thompson,et al.  Organization of memory traces in the mammalian brain. , 1994, Annual review of neuroscience.