Historically the dominant trend in comparative brain and behavior research has emphasized the differences in cognition and its neural basis among species. In fact, the vertebrate forebrain shows a remarkable range of diversity and specialized adaptations. Probably the major morphological variation is that observed in the telencephalon of the actinopterygian fish, which undergoes a process of eversion during embryonic development, relative to the telencephalon of non-actinopterygians (for instance, amniotes), which develops by a process of evagination. These different developmental processes produce notable variation, mainly two solid telencephalic hemispheres separated by a unique ventricle in the actinopterygian radiation that contrasts with the hemispheres with internal ventricles in other groups. However, an increasing amount of evidence reveals that the forebrain of vertebrates, whether everted or evaginated, presents a common pattern of basic organization that supports highly conserved cognitive functions. We analyze here recent data indicating a close functional similarity between spatial cognition mechanisms in different groups of vertebrates, mammals, birds, reptiles, and teleost fish, and we show in addition that they rely on homologous neural mechanisms. Thus, recent functional and behavioral comparative evidence is added to the developmental and neuroanatomical data suggesting that the evolution of cognitive capabilities and their neural basis in vertebrates could have been more conservative than previously realized.

1.
Berthoz A (1999) Hippocampal and parietal contribution to topokinetic and topographic memory. In: The Hippocampal and Parietal Foundations of Spatial Cognition (Burgess N, Jeffery KJ, O’Keefe J, eds), pp 381–403. Oxford: Oxford University Press.
2.
Bingman VP (1992) The importance of comparative studies and ecological validity for understanding hippocampal structure and cognitive function. Hippocampus 2:213–220.
3.
Bingman VP, Mench JA (1990) Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behav Brain Res 40:227–238.
4.
Burgess N, Jeffery KJ, O’Keefe J (1999) The Hippocampal and Parietal Foundations of Spatial Cognition. London: Oxford University Press.
5.
Butler AB, Hodos W (1996) Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. New York: Wiley-Liss.
6.
Carroll R (1988) Vertebrate Paleontology and Evolution. New York: Freeman.
7.
Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272–274.
8.
Day LB, Crews D, Wilczynski W (1999) Relative medial and dorsal cortex volume in relation to foraging ecology in congeneric lizards. Brain Behav Evol 54:314–322.
9.
Deacon TW (1990) Rethinking mammalian brain evolution. Am Zool 30:629–705.
10.
Du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:131–146.
11.
Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nature Rev 1:41–50.
12.
Fremouw T, Jackson-Smith P, Kesner RP (1997) Impaired place learning and unimpaired cue learning in hippocampal-lesioned pigeons. Behav Neurosci 111:963–975.
13.
Fritzsch B, Beisel KW, Bermingham NA (2000) Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11:35–44
14.
Gaffney ES (1980) Phylogenetic relationships of the major groups of amniotes In: The Terrestrial Environment and the Origin of Land Vertebrates (Pancher AL, ed), pp 593–610. London: Academic Press.
15.
Good M (1987) The effects of hippocampal-area parahippocampalis lesions on discrimination learning in the pigeon. Behav Brain Res 31:207–220.
16.
Graziano MSA, Gross CG (1998) Spatial maps for the control of movements. Curr Opinion Neurobiol 8:195–201.
17.
Herrero L, Rodríguez F, Salas C, Torres B (1998) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120:291–305.
18.
Hodos W, Campbell CBG (1969) The scala naturae: Why there is no theory in comparative psychology. Psychol Rev 76:337–350.
19.
Hodos W, Campbell CBG (1990) Evolutionary scales and comparative studies of animal cognition. In: Neurobiology of Comparative Cognition (Kesner RP, Olton DS, eds), pp 1–20. Hillsdale: Lawrence Erlbaum Associates.
20.
Holtzman DA, Harris TW, Aranguren G, Bostock E (1999) Spatial learning of an escape task by young corn snakes, Elaphe guttata guttata. Anim Behav 57:51–60.
21.
Isa T, Sasaki S (2002) Brainstem control of head movements during orienting: organization of the premotor circuits. Prog Neurobiol 66:205–241.
22.
Jiménez-Moya F (2003). Motor areas in the teleostean telencephalon: mapping by electrical microstimulation and cytoarchitectural delimitation. PhD. Doctoral Dissertation (Unpublished). University of Seville.
23.
Karten HJ (1997) Evolutionary development biology meets the brain: The origins of mammalian cortex. Proc Natl Acad Sci USA 94:2800–2804.
24.
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.
25.
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.
26.
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.
27.
López JC, Rodríguez F, Gómez Y, Vargas JP, Broglio C, Salas C (2000c) Place and cue learning in turtles. Anim Learn Behav 28:360–372.
28.
López JC, Gómez Y, Rodríguez F, Broglio C, Vargas JP, Salas C (2001) Spatial learning in turtles. Anim Cogn 4:49–59.
29.
Medina L, Reiner A (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1–12.
30.
Mittelstaedt ML, Glasauer S (1991) Idiothetic navigation in gerbils and humans. Zool J Physiol 95:427–435.
31.
Morris RGM, Garrud P, Rawlins JNP, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683.
32.
Nadel L (1991) The hippocampus and space revisited. Hippocampus 1:221–229.
33.
Nadel L (1994) Multiple memory systems: what and why? An update. In: Memory Systems (Schacter DL, Tulving E, eds), pp. 39–63. Cambridge: MIT Press.
34.
Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates. Berlin: Springer-Verlag.
35.
Northcutt RG (1981) Evolution of the telencephalon in nonmammals. Ann Rev Neurosci 4:301–350.
36.
Northcutt RG (1995) The forebrain of gnathostomes: In search of a morphotype. Brain Behav Evol 46:275–318.
37.
Northcutt RG, Braford MR (1980) New observations on the organization and evolution of the telencephalon of actinopterygian fishes. In: Comparative Neurology of the Telencephalon (Ebbesson SOE, ed), pp 41–98. New York: Plenum Press.
38.
Northcutt RG, Kaas JH (1995) The emergence and evolution of mammalian neocortex. TINS 18:371–426.
39.
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. London: Oxford University Press.
40.
Overmier JB, Hollis KL (1983) The teleostean telencephalon in learning. In: Fish Neurobiology (Northcut RG, Davis RE, eds), pp 265–284. Ann Arbor: The University of Michigan Press.
41.
Paillard J (1991) Motor and representational framing of space. In: Brain and Space (Paillard J, ed), pp 163–182. Oxford: Oxford University Press.
42.
Pearce JM, Roberts ADL, Good M (1998) Hippocampal lesions disrupt a cognitive map but not vector encoding. Nature 996:75–77.
43.
Powers AS (1990) Brain mechanisms of learning in reptiles. In: Neurobiology of Comparative Cognition (Kesner RP, Olton DS, eds), pp 157–177. Hillsdale: Lawrence Erlbaum Associates.
44.
Prechtl JC, von der Emde G, Wolfart J, Karamursel S, Akoev GN, Andrianov YN, Bullock TH (1998) Sensory processing in the pallium of a mormyrid fish. J Neurosci 18:7381–7393.
45.
Rodríguez F, Duran E, Vargas JP, 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.
46.
Rodríguez F, López JC, Vargas JP, Broglio C, Gómez Y, Salas C (2002a) Spatial memory and hippocampal pallium through vertebrate evolution: Insights from reptiles and teleost fish. Brain Res Bull 57:499–503.
47.
Rodríguez F, López JC, Vargas JP, Gómez Y, Broglio C, Salas C (2002b) Conservation of spatial memory function in the pallial forebrain of amniotes and ray-finned fishes. J Neurosci 22:2894–2903.
48.
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
49.
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.
50.
Salas C, Herrero L, Rodríguez F, Torres B (1997) Tectal codification of eye movements in goldfish studied by electrical microstimulation. Neuroscience 78:271–288.
51.
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.
52.
Sherry DF, Vaccarino AL (1989) Hippocampus and memory for food caches in black-capped chickadees. Behav Neurosci 103:308–318.
53.
Simpson JI, Graf W (1985) The selection of reference frames by nature and its investigators. In: Adaptive Mechanisms in Gaze Control. Facts, and Theories (Berthoz A, Jones GM, eds), pp 3–16. Amsterdam: Elsevier.
54.
Sparks DL (2002) The brainstem control of saccadic eye movements. Nature Rev Neurosci 3:952–964.
55.
Stein BE, Meredith MA (1993) The merging of the senses. Cambridge: MIT Press.
56.
Stone A, Ford NB, Holtzman DA (2000) Spatial learning and shelter selection by juvenile spotted phythons, Anteresia maculosus. J Herpetol 34:575–587.
57.
Torres B, Pérez-Pérez MP,Herrero L, Ligero M, Núñez-Abades PA (2002) Neural substrate underlying tectal eye movement codification in goldfish. Brain Res Bull 57:345–348.
58.
Ulinski PS (1990) The cerebral cortex of reptiles. In: Cerebral Cortex: Vol 8A. Comparative Structure and Evolution of the Cerebral Cortex (Jones EG, Peters A, eds), pp 139–215. New York: Plenum Press.
59.
Vanegas H (1984) Comparative neurology of the optic tectum. New York: Plenum Press.
60.
Vargas JP, Rodríguez F, López 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.
61.
Wiley EO (1981) Phylogenetics. The theory and practice of phylogenetic systematics. New York: Wiley.
62.
Wullimann MF, Rink E (2002) The teleostean forebrain: a comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization. Brain Res Bull 57:363–370.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.