Brain Evolution and Comparative Neuroanatomy

Alice S Powers, Stony Brook University, Stony Brook, New York, USA

Published online: November 2014

DOI: 10.1002/9780470015902.a0000088.pub3

Abstract

Brains have many diverse forms in different animal groups, from complex layered structures to simple nerve nets. The range of different brain forms is reflective of the huge variety of environmental niches and lifestyles in which organisms have been successful. Both simple and elaborate brains are adaptive, depending on the selective pressures to which organisms are subjected. In vertebrates, a basic plan can be recognised across groups, especially in the brainstem, but the forebrain of birds and mammals is much more elaborate than those of other vertebrates. Elaborate nervous systems have developed independently in some molluscs, arthropods and vertebrates. Correlated with this elaboration is the capacity for complex learning, which is highly developed in some molluscs, arthropods and birds and mammals. The presence of elaborated brains in disparate groups illustrates that evolution of the brain has not shown a trend from simple to complex, but rather has occurred independently in different lineages.

Key Concepts:

  • Two structures are homologous if they can be traced to a common ancestor. Because brains do not fossilise, establishment of brain homologies requires as much information as possible about the similarities between brains of different groups.

  • There is no trend in the evolution of the brain. Specialisations in brain traits develop in response to the demands of various environmental selective pressures. Many animals with simple nervous systems are very successful.

  • Two major groups of invertebrates can be distinguished: those with radial symmetry and those with bilateral symmetry. Those with radial symmetry have simple nervous systems with a ring of neurons, while bilaterally symmetrical organisms have concentrations of neurons in the head region.

  • Octopi, insects and crustaceans have elaborate brains, well‐developed eyes and extensive learning ability, rivalling that of mammals.

  • The brains of the earliest chordate ancestors of vertebrates had bilateral eyes, a diencephalon and hindbrain.

  • All vertebrates have the same subdivisions of the brain: the hindbrain, midbrain and forebrain (the diencephalon and telencephalon). The hindbrain is relatively conservative, retaining a recognisable structure in spite of many variations, whereas the forebrain shows more variability among vertebrate groups.

  • Twenty‐five cranial nerves can be recognised in vertebrates, innervating muscles of the head and specialized sense organs, including lateral line organs and taste buds on the body surface.

  • The vertebrate telencephalon includes a dorsal pallial area which differentiates into the cerebral cortex in mammals, but there is disagreement about the homologous areas in nonmammals.

  • Brains have evolved to enable organisms to compete successfully in different environmental niches and the adaptations they show reflect the demands of those environments.

Keywords: evolution of brain; insect brain; nerve net; octopus; vertebrate brain; telencephalon; fish; reptile; bird; pallium

Figure 1.

A cross section through the brain of an insect. The protocerebrum, deutocerebrum, tritocerebrum and optic lobes can be seen. The gnathal ganglia comprise the mandibular, maxillary and labial ganglia. Adapted from Ito et al. (), courtesy of Laura Powers.
Figure 2.

Lateral view of the brain of a generalised ray‐finned fish. Rostral is towards the left and dorsal is towards the top. The optic tract forms the lateral surface of the diencephalon, and the optic tectum, which is called the superior colliculus in mammals, is a major component of the mesencephalon. In this view, the optic tectum conceals the auditory relay part of the midbrain roof, called the torus semicircularis in many nonmammals and the inferior colliculus in mammals. The hindbrain includes the cerebellum and the brainstem caudal to the midbrain.
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References

Bozorgmehr T, Ardiel EL, McEwan AH and Rankin CH (2013) Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit. Frontiers in Physiology 4(88): 1–11.

Bruce LL and Neary TJ (1995) The limbic system of tetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behavior and Evolution 46(4–5): 224–234.

Butler AB (1995) The dorsal thalamus of jawed vertebrates: a comparative viewpoint. Brain, Behavior and Evolution 46(4–5): 209–223.

Butler AB and Hodos W (2005) Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, 2nd edn. Hoboken NJ: Wiley.

Butler AB, Reiner A and Karten HJ (2011) Evolution of the amniote pallium and the origins of mammalian neocortex. Annals of the New York Academy of Sciences 1225: 14–27.

Depew MJ and Olsson L (2008) Symposium on the evolution and development of the vertebrate head. Journal of Experimental Zoology B Molecular and Developmental Evolution 310B(4): 287–293.

Dugas‐Ford J, Rowell JJ and Ragsdale CW (2012) Cell‐type homologies and the origins of the neocortex. Proceedings of the National Academy of Sciences USA 109(42): 16974–16979.

Eisthen HL (1997) Evolution of vertebrate olfactory systems. Brain, Behavior and Evolution 50(4): 222–233.

Finger TE (2008) Sorting food from stones: the vagal taste system in goldfish, Carassius auratus. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 194(2): 135–143.

Firth BT, Christian KA, Belan I and Kennaway DJ (2010) Melatonin rhythms in the Australian freshwater crocodile (Crocodylus johnstoni): a reptile lacking a pineal complex? Journal of Comparative Physiology B 180(1): 67–72.

Gans C and Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220(4594): 268–274.

Hawkins RD, Kandel ER and Bailey CH (2006) Molecular mechanisms of memory storage in Aplysia. Biological Bulletin 210(3): 174–191.

Hikosaka O (2010) The habenula: from stress evasion to value‐based decision‐making. Nature Reviews Neuroscience 11(7): 503–513.

Hochner B (2012) An embodied view of octopus neurobiology. Current Biology 22(20): R887–R892.

Ito K, Shinomiya K, Ito M et al. (2013) A systematic nomenclature for the insect brain. Neuron 81(4): 755–765.

Johnson MC and Wuensch KL (1994) An investigation of habituation in the jellyfish Aurelia aurita. Behavioural and Neural Biology 61(1): 54–59.

Krauzlis RJ, Lovejoy LP and Zénon A (2013) Superior colliculus and visual spatial attention. Annual Review of Neuroscience 36: 165–182.

Laberge F, Muhlenbrock‐Lenter S, Dicke U and Roth G (2008) Thalamo‐telencephalic pathways in the fire‐bellied toad Bombina orientalis. Journal of Comparative Neurology 508(5): 806–823.

Laberge F, Mühlenbrock‐Lenter S, Grunwald W and Roth G (2006) Evolution of the amygdala: new insights from studies in amphibians. Brain, Behavior, and Evolution 67(4): 177–187.

Lopez JC, Vargas JP, Gomez Y and Salas C (2003) Spatial and non‐spatial learning in turtles: the role of medial cortex. Behavioural Brain Research 143(2): 109–120.

Mallatt J and Chen J‐Y (2003) Fossil sister group of craniates: predicted and found. Journal of Morphology 258: 1–31.

Medina L, Abellan A, Vicario A and Desfilis E (2014) Evolutionary and developmental contributions for understanding the organization of the basal ganglia. Brain, Behavior, and Evolution 83(2): 112–125.

Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nature Reviews Neuroscience 13(11): 758–768.

Montgomery JC, Bodznick D and Yopak KE (2012) The cerebellum and cerebellum‐like structures of cartilaginous fishes. Brain, Behavior, and Evolution 80(2): 152–165.

Nauta WJH and Karten HJ (1970) A general profile of the vertebrate brain with sidelights on the ancestry of the cerebral cortex. In: Schmitt FO (ed.), The Neurosciences: Second Study Section, pp. 1–26. New York, NY: Rockefeller University Press.

Northcutt RG (1996) The Agnathan ark: the origin of craniate brains. Brain, Behavior, and Evolution 48(5): 237–247.

Northcutt RG (2005) The new head hypothesis revisited. Journal of Experimental Zoology B Molecular and Developmental Evolution 304B(4): 274–297.

Northcutt RG (2011) Do teleost fishes possess a homolog of mammalian isocortex? Brain, Behavior, and Evolution 78(2): 136–138.

Northcutt RG and Gonzalez A (2011) A reinterpretation of the cytoarchitectonics of the telencephalon of the Comoran coelacanth. Frontiers in Neuroanatomy 5(9): 1–7.

Perez‐Fernandez J, Stephenson‐Jones M, Suryanarayana SM, Robertson B and Grillner S (2014) Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. Journal of Comparative Neurology. doi:10.1002/cne.23639 [Epub ahead of print].

Pombal MA, Alvarez‐Otero R, Perez‐Fernandez J, Solveira C and Megias M (2011) Development and organization of the lamprey telencephalon with special reference to the GABAergic system. Frontiers in Neuroanatomy 5(20): 1–12.

Pombal MA, El Manira A and Grillner S (1997) Afferents of the lamprey striatum with special reference to the dopaminergic system: a combined tracing and immunohistochemical study. Journal of Comparative Neurology 386: 71–91.

Puelles L, Kuwana E, Bulfone A et al. (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx‐2, Emx‐1, Nkx‐2.1, Pax‐6, and Tbr‐1. Journal of Comparative Neurology 424(3): 409–438.

Rodríguez F, López JC, Vargas JP et al. (2002) Conservation of spatial memory function in the pallial forebrain of reptiles and ray‐finned fishes. Journal of Neuroscience 22(7): 2894–2903.

Satterlie RA (2011) Do jellyfish have central nervous systems? Journal of Experimental Biology 214(8): 1215–1223.

Schuchert P (1993) Trichoplax adhaerens (Phylum Placozoa) has cells that react with antibodies against neuropeptide RFamide. Acta Zoologica 74(2): 115–117.

Shomrat T, Zarrella I, Fiorito G and Hochner B (2008) The octopus vertical lobe modulates short‐term learning rate and uses LTP to acquire long‐term memory. Current Biology 18(5): 337–342.

Stephenson‐Jones M, Floros O, Robertson B and Grillner S (2012) Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5‐hydroxytryptophan (5‐HT) systems. Proceedings of the National Academy of Sciences 109(3): E164–E173.

Stephenson‐Jones M, Samuelsson E, Ericsson J, Robertson B and Grillner S (2011) Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Current Biology 21(13): 1081–1091.

Striedter GF (1997) The telencephalon of tetrapods in evolution. Brain, Behavior, and Evolution 49(4): 179–213.

Swanson LW and Petrovich GD (1998) What is the amygdala? Trends in Neurosciences 21(8): 323–331.

Vargas JP, Petruso EJ and Bingman VP (2004) Hippocampal formation is required for geometric navigation in pigeons. European Journal of Neuroscience 20(7): 1937–1944.

Vassas A, Bourdy G, Paillard JJ et al. (1996) Naturally occurring somatostatin and vasoactive intestinal peptide inhibitors. Isolation of alkaloids from two marine sponges. Planta Medica 62(1): 28–30.

Vígh B, Manzano MJ, Zádori A et al. (2002) Nonvisual photoreceptors of the deep brain, pineal organs and retina. Histology and Histopathology 17(2): 555–590.

Wang Y, Brzozowska‐Prechtl A and Karen HJ (2010) Laminar and columnar auditory cortex in avian brain. Proceedings of the National Academy of Sciences USA 107(28): 12676–12681.

White JG, Southgate E, Thomson JN and Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B Biological Sciences 314(1165): 1–340.

Further Reading

Allman JM (1999) Evolving Brains. New York, NY: Scientific American Library.

Balda RP, Pepperberg IM and Kamil AC (eds) (1998) Animal Cognition in Nature: The Convergence of Psychology and Biology in Laboratory and Field. San Diego, CA: Academic Press.

Breidbach O and Kutsch W (eds) (1995) The Nervous System of Invertebrates: An Evolutionary and Comparative Approach. Basel: Birkhäuser.

Demski L (2013) Evolution of brain complexity and animal minds. 24th Annual Karger Workshop. Brain, Behavior, and Evolution 82(1): 1–79.

Kaas JH (ed.) (2009) Evolutionary Neuroscience. Oxford: Elsevier.

Nieuwenhuys R, ten Donkelaar HJ and Nicholson C (1998) The Central Nervous System of Vertebrates. Berlin: Springer.

Papini MR (2008) Comparative Psychology: Evolution and Development of Behavior, 2nd edn. New York, NY: Psychology Press.

Roth G (2013) The Long Evolution of Brains and Minds. Berlin: Springer.

Strausfeld NJ (2012) Arthropod Brains: Evolution, Functional Elegance, and Historical Significance. Cambridge, MA: Harvard University Press.

Striedter GF (2004) Principles of Brain Evolution. Sunderland, MA: Sinauer Associates.

Related Sub-Topics:

Physiological Ecology | Evolutionary Ecology | Adaptive Evolution | Evolution and Development | Macroevolution | Organisation of the Nervous System | Development of Invertebrate Nervous System | Development of Vertebrate Nervous System | Diversification of Plants and Animals | Evolution of Novelty
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Article Title: Brain Evolution and Comparative Neuroanatomy
 
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Powers, Alice S(Nov 2014) Brain Evolution and Comparative Neuroanatomy. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000088.pub3]