Parcellation and Area-Area Connectivity as a Function of Neocortex SizeChangizi M.A.a · Shimojo S.b, c
aSloan-Swartz Center for Theoretical Neurobiology, Caltech, and bDivision of Biology, Computation and Neural Systems, Pasadena, Calif., USA; cNTT Communication Science Laboratory, Atsugi, Kanagawa, Japan
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Article / Publication Details
Via the accumulation of data from across the neuroanatomy literature, we estimate the manner in which (i) the number of neocortical areas varies with neocortex size, and (ii) the number of area-area connections varies with neocortex size. Concerning parcellation, we find that the number of areas scales approximately as the 1/3 power of gray matter volume, or, equivalently, as the square root of the total number of neocortical neurons. A consequence of this is that the average number of neurons per area also scales approximately as the square root of the total number of areas. Concerning area-area connectivity, we find evidence that the total number of area-area connections scales as the square of the number of areas. These scaling results help constrain theories about the principles underlying neocortical organization.
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Abeles M (1991) Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge: Cambridge University Press.
- Aboitiz F (1996) Does bigger mean better? Evolutionary determinants of brain size and structure. Brain Behav Evol 47:225–245.
Allman JM (1999) Evolving Brains. New York: Sci Am Lib.
- Barlow HB (1986) Why have multiple cortical areas? Vis Res 26:81–90.
- Beck PD, Kaas JH (1998a) Cortical connections of the dorsomedial visual area in new world owl monkeys (Aotus trivergatus) and squirrel monkeys (Saimiri sciureus). J Comp Neurol 400:18–34.
- Beck PD, Kaas JH (1998b) Cortical connections of the dorsomedial visual area in prosimian primates. J Comp Neurol 398:162–178.
- Beck PD, Pospichal MW, Kaas JH (1996) Topography, architecture, and connections of somatosensory cortex in opossums: evidence for five somatosensory areas. J Comp Neurol 366:109–133.
Braitenberg V (1978) Cortical architectonics, general and areal. In: Architectonics of the Cerebral Cortex (Brazier M, Petsche H, eds), pp 443–465. New York: Raven Press.
- Braitenberg V (2001) Brain size and number of neurons: An exercise in synthetic neuroanatomy. J Comp Neurosci 10:71–77.
Braitenberg V, Schuz A (1998) Cortex: Statistics and Geometry of Neuronal Connectivity. Heidelberg: Springer-Verlag.
- Catania KC, Lyon DC, Mock OB, Kaas JH (1999) Cortical organization in shrews: Evidence from five species. J Comp Neurol 410:55–72.
- Changizi MA (2001) Principles underlying mammalian neocortical scaling. Biol Cybern 84:207–215.
- Changizi MA (2003a) The relationship between number of muscles, behavioral repertoire, and encephalization in mammals. J Theor Biol 220:157–168.
Changizi MA (2003b) The Brain from 25,000 Feet: High Level Explorations of Brain Complexity, Perception, Induction and Vagueness. Dordrecht: Kluwer Academic.
Changizi MA (2005a) Scaling the brain and its connections. In: Evolution of Nervous Systems (Kaas JH, ed). Oxford UK: Elsevier.
Changizi MA (2005b) The optimal primate ventral stream from estimates of the complexity of visual objects. Under review.
Changizi MA, He D (2005) Four correlates of complex behavioral networks: differentiation, behavior, connectivity, and compartmentalization. Complexity, in press.
- Cherniak C, Changizi MA, Kang D (1999). Large-scale optimization of neuron arbors. Physical Rev E 59:6001–6009.
- Collins CE, Stepniewska I, Kaas JH (2001) Topographic patterns of V2 cortical connections in a prosimian primate (Galago garnetti). J Comp Neurol 431:155–167.
- Coogan TA, Burkhalter A (1993) Hierarchical organization of areas in rat visual cortex. J Neurosci 13:3749–3772.
- Cowey A (1979) Cortical maps and visual perception. The Grindley Memorial Lecture. Q J Exp Psychol 31:1–17.
Cowey A (1981) Why are there so many visual areas? In: The Organization of the Cerebral Cortex. (Schmitt FO, Warden FG, Adelman G, Dennis SG, eds), pp 395–413. Cambridge MA: MIT Press.
Crile G, Quiring DP (1940) A record of the body weight and certain organ and gland weights of 3690 animals. Ohio J Sci 40:219–259.
- Durbin R, Mitchison G (1990) A dimension reduction framework for understanding cortical maps. Nature 343:644–647.
- Fabri M, Burton H (1991) Ipsilateral cortical connections of primary somatic sensory cortex in rats. J Comp Neurol 311:405–424.
- Frahm HD, Stephan H, Baron G (1984) Comparison of brain structure volumes in insectivora and primates. V. Area striata (AS). J Hirnforsch 25:537–557.
Garey LJ (1999) Brodmann’s ‘Localisation in the Cerebral Cortex’. London: Imperial College Press.
- Hackett TA, Stepniewska I, Kaas JH (1998) Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 394:475–495.
- Harrison KH, Hof PR, Wang SS-H (2002) Scaling laws in the mammalian neocortex: Does form provide clues to function? J Neurocytol 31:289–298.
- Haug H (1987) Brain sizes, surfaces and neuronal sizes of the cortex cerebri: A stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat 180:126–142.
- Hofman MA (1982) Encephalization in mammals in relation to the size of the cerebral cortex. Brain Behav Evol 20:84–96.
- Hofman MA (1985) Size and shape of the cerebral cortex in mammals. I. The cortical surface. Brain Behav Evol 27:28–40.
- Hofman MA (1989) On the evolution and geometry of the brain in mammals. Prog Neurobiol 32:137–158.
- Hofman MA (1991) The fractal geometry of convoluted brains. J Hirnforsch 32:103–111.
Hrdlicka A (1907) Brain weight in vertebrates. Smithsonian Miscellaneous Collections, pp 89–112. Washington DC: Smithsonian.
- Jacobs RA, Jordan MI (1992) Computational consequences of a bias toward short connections. J Cogn Neurosci 4:323–336.
Jerison HJ (1973) Evolution of the Brain and Intelligence. New York: Academic Press.
Jerison HJ (1982) Allometry, brain size, cortical surface, and convolutedness. In: Primate Brain Evolution (Armstrong E, Falk D, eds), pp 77–84. New York: Plenum Press.
Kaas JH (1977) Sensory representations in mammals. In: Function and Formation of Neural Systems (Stent GS, ed), pp 65–80. Berlin: Dahlem Konferenzen.
- Kaas JH (1987) The organization of neocortex in mammals: implications for theories of brain function. Ann Rev Psychol 38:129–151.
- Kaas JH (1989) Why does the brain have so many visual areas? J Cogn Neurosci 1:121–135.
- Kaas JH (1995) The evolution of isocortex. Brain Behav Evol 46:187–196.
- Kaas JH (1997) Topographic maps are fundamental to sensory processing. Brain Res Bull 44:107–112.
- Kaas JH (2000) Why is brain size so important: design problems and solutions as neocortex gets bigger or smaller. Brain Mind 1:7–23.
- Kaas JH, Krubitzer LA, Johanson KL (1989) Cortical connections of areas 17 (V-1) and 18 (V-II) of squirrels. J Comp Neurol 281:426–446.
- Kaas JH, Hackett TA (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci 97:11793–11799.
- Kahn DM, Huffman KJ, Krubitzer L (2000) Organization and connections of V1 in Monodelphis domestica. J Comp Neurol 428:337–354.
- Kingsbury MA, Finlay BL (2001) The cortex in multidimensional space: where do cortical areas come from? Dev Sci 4:125–157.
- Krubitzer L (1995) The organization of neocortex in mammals: are species differences really so different? Trends Neurosci 18:408–417.
- Krubitzer LA, Calford MB, Schmid LM (1993) Connections of somatosensory cortex in megachiropteran bats: the evolution of cortical fields in mammals. J Comp Neurol 327:473–506.
- Krubitzer L, Huffman KJ (2000) Arealization of the neocortex in mammals: genetic and epigenetic contributions to the phenotype. Brain Behav Evol 55:322–355.
- Krubitzer LA, Kaas JH (1990a) Cortical connections of MT in four species of primates: areal, modular, and retinotopic patterns. Vis Neurosci 5:165–204.
- Krubitzer LA, Kaas JH (1990b) The organization and connections of somatosensory cortex in marmosets. J Neurosci 10:952–974.
- Krubitzer L, Künzle H, Kaas J (1997) Organization of sensory cortex in a madagascan insectivore, the tenrec (Echinops telfairi). J Comp Neurol 379:399–414.
- Krubitzer L, Manger P, Pettigrew J, Calford M (1995) Organization of somatosensory cortex in monotremes: in search of a prototypical plan. J Comp Neurol 351:261–306.
- Krubitzer LA, Sesma MA, Kaas JH (1986) Microelectrode maps, myeloarchitecture, and cortical connections of three somatotopically organized representations of the body surface in the parietal cortex of squirrels. J Comp Neurol 250:403–430.
- Lewis JW, van Essen DC (2000) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol 428:112–137.
- Lyon DC, Jain N, Kaas JH (1998) Cortical connections of striate and extrastriate visual areas in tree shrews. J Comp Neurol 401:109–128.
- Lyon DC, Kaas JH (2001) Connectional and architectonic evidence for dorsal and ventral V3, and dorsomedial area in marmoset monkeys. J Neurosci 21:249–261.
- Lyon DC, Kaas JH (2002a) Connectional evidence for dorsal and ventral V3, and other extrastriate areas in the prosimian primate, Galago gernetti. Brain Behav Evol 59:114–129.
- Lyon DC, Kaas JH (2002b) Evidence from V1 connections for both dorsal and ventral subdivisions of V3 in three species of new world monkeys. J Comp Neurol 449:281–297.
- Manger PR, Kiper D, Masiello I, Murillo L, Tettoni L, Hunyadi Z, Innocenti GM (2002) The representation of the visual field in three extrastriate areas of the ferret (Mustela putorius) and the relationship of retinotopy and field boundaries to callosal connectivity. Cereb Cortex 12:423–437.
- Mitchison G (1991) Neuronal branching patterns and the economy of cortical wiring. Proc R Soc Lond B 245:151–158.
- Mitchison G (1992) Axonal trees and cortical architecture. Trends Neurosci 15:122–126.
Nowak RM (1999) Walker’s Mammals of the World. Baltimore MD: The Johns Hopkins University Press.
- Northcutt RG, Kaas JH (1995) The emergence and evolution of mammalian neocortex. Trends Neurosci 18:373–379.
- Passingham RE (1973) Anatomical differences between the neocortex of man and other primates. Brain Behav Evol 7:337–359.
- Prothero J (1997a) Cortical scaling in mammals: A repeating units model. J Brain Res 38:195–207.
- Prothero J (1997b) Scaling of cortical neuron density and white matter volume in mammals, J Brain Res 38:513–524.
- Prothero JW, Sundsten JW (1984) Folding of the cerebral cortex in mammals. Brain Behav Evol 24:152–167.
- Ringo JL (1991) Neuronal interconnection as a function of brain size. Brain Behav Evol 38:1–6.
- Ringo JL, Doty RW, Demeter S, Simard PY (1994) Time is of the essence: A conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cereb Cortex 4:331–343.
- Rosa MGP, Schmid LM, Krubitzer LA, Pettigrew JD (1993) Retinotopic organization of the primary visual cortex of flying foxes (Pteropus poliocephalus and Pteropus scapulatus). J Comp Neurol 335:55–72.
- Scannell JW, Young MP (1993) The connectional organization of neural systems in the cat cerebral cortex. Curr Biol 3:191–200.
- Scannell JW, Blakemore C, Young MP (1995) Analysis of connectivity in the cat cerebral cortex. J Neurosci 15:1463–1483.
Sherwani N (1995) Algorithms for VLSI Physical Design Automation. Boston: Kluwer Academic.
Shultz JR, Wang SS-H (2001) How the neocortex got its folds: Ultrastructural parameters underlying macroscopic features. Soc Neurosci Abstracts.
Snow RL, Nelson A, Driscoll LL, Hartman KL, Silveira LCL, Finlay BL (1997) Scaling of the visual system, photoreceptors to extrastriate cortex, emphasizing primates. Soc Neurosci Abstracts 23:1308.
- Stephan H, Frahm H, Baron G (1981) New and revised data on volumes of brain structures in insectivores and Primates. Folia Primatol 35:1–29.
Stephan H ‘The Stephan Collection.’ http://turing.commtechlab.msu.edu/default.htm
- Stevens CF (2001) An evolutionary scaling law for the primate visual system and its basis in cortical function. Nature 411:193–195.
- Tower DB (1954) Structural and functional organization of mammalian cerebral cortex: The correlation of neurone density with brain size. J Comp Neurol 101: 9–52.
- Tower DB, Elliott KAC (1952) Activity of acetylcholine system in cerebral cortex of various unanesthetized mammals. Am J Physiol 168: 747–759.
- Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385: 313–319.
- Von Bonin G (1937) Brain-weight and body-weight of mammals. J Gen Psych 16:379–389.
- Young MP (1993) The organization of neural systems in the primate cerebral cortex. Proc R Soc Lond B 252:13–18.
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