Biological Theory

, Volume 14, Issue 1, pp 1–20 | Cite as

Neural Reuse and the Modularity of Mind: Where to Next for Modularity?

  • John ZerilliEmail author


The leading hypothesis concerning the “reuse” or “recycling” of neural circuits builds on the assumption that evolution might prefer the redeployment of established circuits over the development of new ones. What conception of cognitive architecture can survive the evidence for this hypothesis? In particular, what sorts of “modules” are compatible with this evidence? I argue that the only likely candidates will, in effect, be the columns which Vernon Mountcastle originally hypothesized some 60 years ago, and which form part of the well-known columnar hypothesis in neuroscience—systems that cannot handle gross cognitive functions (vision, olfaction, language, etc.) as distinct from strictly exiguous subfunctions (such as aspects of edge detection, depth discrimination, etc.). This is in stark contrast to the modules postulated by much of cognitive psychology, cognitive neuropsychology, and evolutionary psychology. And yet the fate of this revised notion is unclear. The main issue confronting it is the effect of the neural network context on local function. At some point the effects of context are so strong that the degree of specialization required for modularity is not able to be met. Still, despite indications from neuroimaging that peripheral and central systems deploy shared circuitry, some skills clearly do seem to display modularization and autonomy. This article: (1) provides an in-depth analytical and historical review of the fortunes of modular thinking in cognitive science; (2) offers a systematic calibration of brain regions in terms of degrees of functional specificity and robustness; and (3) suggests another way of accounting for the partially encapsulated character of expertise and other highly practiced skills without having to resort to domain-specific modules.


Cognitive dissociations Cortical column Modularity Neural redundancy Neural reuse 



This research was supported by an Australian Government Research Training Program Scholarship.


  1. Ackerman JM, Nocera CC, Bargh JA (2010) Incidental haptic sensations influence social judgments and decisions. Science 328:1712–1715CrossRefGoogle Scholar
  2. Altun ZF, Hall DH (2011) Nervous system, general description. In: Altun ZF, Herndon LA, Crocker C et al. (eds) WormAtlas
  3. Amaral DG, Strick PL (2013) The organization of the central nervous system. In: Kandel ER, Schwartz JH, Jessell TM et al (eds) Principles of neural science. McGraw-Hill, New York, pp 337–355Google Scholar
  4. Anderson ML (2007a) Evolution of cognitive function via redeployment of brain areas. Neuroscientist 13:13–21CrossRefGoogle Scholar
  5. Anderson ML (2007b) Massive redeployment, exaptation, and the functional integration of cognitive operations. Synthese 159(3):329–345CrossRefGoogle Scholar
  6. Anderson ML (2007c) The massive redeployment hypothesis and the functional topography of the brain. Philos Psychol 21(2):143–174CrossRefGoogle Scholar
  7. Anderson ML (2008) Circuit sharing and the implementation of intelligent systems. Connect Sci 20(4):239–251CrossRefGoogle Scholar
  8. Anderson ML (2010) Neural reuse: a fundamental organizational principle of the brain. Behav Brain Sci 33(4):245–266; discussion 266–313. CrossRefGoogle Scholar
  9. Anderson ML (2014) After phrenology: neural reuse and the interactive brain. MIT Press, CambridgeCrossRefGoogle Scholar
  10. Anderson ML, Finlay BL (2014) Allocating structure to function: the strong links between neuroplasticity and natural selection. Front Hum Neurosci 7:1–16CrossRefGoogle Scholar
  11. Bach-y-Rita P (2004) Emerging concepts of brain function. J Integr Neurosci 4(2):183–205CrossRefGoogle Scholar
  12. Bargh JA, Williams LE, Huang JY et al (2010) From the physical to the psychological: mundane experiences influence social judgment and interpersonal behavior. Behav Brain Sci 33(4):267–268CrossRefGoogle Scholar
  13. Barrett HC (2006) Modularity and design reincarnation. In: Carruthers P, Laurence S, Stich SP (eds) The innate mind volume 2: culture and cognition. Oxford University Press, New York, pp 199–217Google Scholar
  14. Barrett HC, Kurzban R (2006) Modularity in cognition: framing the debate. Psychol Rev 113(3):628–647CrossRefGoogle Scholar
  15. Bechtel W (2008) Mental mechanisms: philosophical perspectives on cognitive neuroscience. Routledge, LondonGoogle Scholar
  16. Bergeron V (2007) Anatomical and functional modularity in cognitive science: shifting the focus. Philos Psychol 20(2):175–195CrossRefGoogle Scholar
  17. Berwick RC, Chomsky N (2016) Why only us: language and evolution. MIT Press, CambridgeCrossRefGoogle Scholar
  18. Binkofski F, Amunts K, Stephan KM et al (2000) Broca’s region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Hum Brain Mapp 11:273–285CrossRefGoogle Scholar
  19. Bressler SL (1995) Large-scale cortical networks and cognition. Brain Res Rev 20:288–304CrossRefGoogle Scholar
  20. Burnston DC (2016) A contextualist approach to functional localization in the brain. Biol Philos 31:527–550CrossRefGoogle Scholar
  21. Buxhoeveden DP, Casanova MF (2002) The minicolumn hypothesis in neuroscience. Brain 125:935–951CrossRefGoogle Scholar
  22. Carruthers P (2006) The architecture of the mind: massive modularity and the flexibility of thought. Oxford University Press, OxfordCrossRefGoogle Scholar
  23. Carruthers P (2008) Précis of the architecture of the mind: massive modularity and the flexibility of thought. Mind Lang 23(3):257–262CrossRefGoogle Scholar
  24. Casasanto D, Dijkstra K (2010) Motor action and emotional memory. Cognition 115(1):179–185CrossRefGoogle Scholar
  25. Chomsky N (1980) Rules and representations. Columbia University Press, New YorkCrossRefGoogle Scholar
  26. Chomsky N (1988) Language and problems of knowledge: the managua lectures. MIT Press, CambridgeGoogle Scholar
  27. Chomsky N (2002) On nature and language. Cambridge University Press, New YorkCrossRefGoogle Scholar
  28. Coase RH (1937) The nature of the firm. Economica New Series 4(16):386–405CrossRefGoogle Scholar
  29. Cole MW, Reynolds JR, Power JD et al (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16(9):1348–1355CrossRefGoogle Scholar
  30. Coltheart M (2011) Methods for modular modelling: additive factors and cognitive neuropsychology. Cogn Neuropsychol 28(3–4):224–240CrossRefGoogle Scholar
  31. Cosmides L, Tooby J (1994) Origins of domain specificity: the evolution of functional organization. In: Hirschfield L, Gelman S (eds) Mapping the world: domain specificity in cognition and culture. Cambridge University Press, New York, pp 85–116CrossRefGoogle Scholar
  32. Craver CF (2007) Explaining the brain. Oxford University Press, OxfordCrossRefGoogle Scholar
  33. da Costa NM, Martin KAC (2010) Whose cortical column would that be? Front Neuroanat 4(5):1–10Google Scholar
  34. Damasio AR, Tranel D (1993) Nouns and verbs are retrieved with differently distributed neural systems. Proc Natl Acad Sci USA 90:4957–4960CrossRefGoogle Scholar
  35. Damasio H, Grabowski TJ, Tranel D et al (1996) A neural basis for lexical retrieval. Science 380:499–505Google Scholar
  36. Deacon TW (2010) A role for relaxed selection in the evolution of the language capacity. Proc Natl Acad Sci USA 107:9000–9006CrossRefGoogle Scholar
  37. Decety J, Grèzes J, Costes N et al (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 120(10):1763–1777CrossRefGoogle Scholar
  38. Dehaene S (2005) Evolution of human cortical circuits for reading and arithmetic: the “neuronal recycling” hypothesis. In: Dehaene S, Duhamel JR, Hauser MD, Rizzolatti G (eds) From monkey brain to human brain. MIT Press, Cambridge, pp 133–157CrossRefGoogle Scholar
  39. Dehaene S, Bossini S, Giraux P (1993) The mental representation of parity and numerical magnitude. J Exp Psychol Gen 122:371–396CrossRefGoogle Scholar
  40. Edelman GM, Gally JA (2001) Degeneracy and complexity in biological systems. Proc Natl Acad Sci USA 98(24):13763–13768CrossRefGoogle Scholar
  41. Fedorenko E, Thompson-Schill SL (2014) Reworking the language network. Trends Cogn Sci 18(3):120–126CrossRefGoogle Scholar
  42. Fedorenko E, Behr MK, Kanwisher N (2011) Functional specificity for high-level linguistic processing in the human brain. Proc Natl Acad Sci USA 108(39):16428–16433CrossRefGoogle Scholar
  43. Fodor JA (1983) The modularity of mind: an essay on faculty psychology. MIT Press, CambridgeGoogle Scholar
  44. Frost R, Armstrong BC, Siegelman N, Christiansen MH (2015) Domain generality versus modality specificity: the paradox of statistical learning. Trends Cogn Sci 19(3):117–125CrossRefGoogle Scholar
  45. Gall FJ, Spurzheim JC (1835) On the function of the brain and each of its parts. Marsh Capen and Lyon, BostonGoogle Scholar
  46. Gauthier I, Curran T, Curby KM, Collins D (2003) Perceptual interference supports a non-modular account of face processing. Nat Neurosci 6(4):428–432CrossRefGoogle Scholar
  47. Gazzaniga MS (1989) Organization of the human brain. Science 245(4921):947–952CrossRefGoogle Scholar
  48. Gilbert CD (2013) The constructive nature of visual processing. In: Kandel ER, Schwartz JH, Jessell TM et al (eds) Principles of neural science. McGraw-Hill, New York, pp 556–576Google Scholar
  49. Glenberg AM, Kaschak MP (2002) Grounding language in action. Psychon Bull Rev 9:558–565CrossRefGoogle Scholar
  50. Glenberg AM, Brown M, Levin JR (2007) Enhancing comprehension in small reading groups using a manipulation strategy. Contemp Educ Psychol 32:389–399CrossRefGoogle Scholar
  51. Glenberg AM, Sato M, Cattaneo L (2008) Use-induced motor plasticity affects the processing of abstract and concrete language. Curr Biol 18(7):R290–R291CrossRefGoogle Scholar
  52. Godfrey-Smith P (2001) Three kinds of adaptationism. In: Orzack SH, Sober E (eds) Adaptationism and optimality. Cambridge University Press, Cambridge, pp 335–357CrossRefGoogle Scholar
  53. Gold I, Roskies AL (2008) Philosophy of neuroscience. In: Ruse M (ed) The oxford handbook of philosophy of biology. Oxford University Press, New York, pp 349–380Google Scholar
  54. Graziano MSA, Taylor CSR, Moore T, Cooke DF (2002) The cortical control of movement revisited. Neuron 36:349–362CrossRefGoogle Scholar
  55. Guida A, Campitelli G, Gobet F (2016) Becoming an expert: ontogeny of expertise as an example of neural reuse. Behav Brain Sci 39:13–15CrossRefGoogle Scholar
  56. Hubbard EM, Piazza M, Pinel P, Dehaene S (2005) Interactions between number and space in parietal cortex. Nat Rev Neurosci 6(6):435–448CrossRefGoogle Scholar
  57. Iriki A, Taoka M (2012) Triadic (ecological, neural, cognitive) niche construction: a scenario of human brain evolution extrapolating tool use and language from the control of reaching actions. Philos Trans R Soc B 367:10–23CrossRefGoogle Scholar
  58. Jacobs JA (1999) Computational studies of the development of functionally specialized neural modules. Trends Cogn Sci 3(1):31–38CrossRefGoogle Scholar
  59. Jungé JA, Dennett DC (2010) Multi-use and constraints from original use. Behav Brain Sci 33(4):277–278CrossRefGoogle Scholar
  60. Kaan E, Stowe LA (2002) Storage and computation in the brain: A neuroimaging perspective. In: Nooteboom SG, Weerman F, Wijnen FNK (eds) Storage and computation in the language faculty. Kluwer, Dordrecht, pp 257–298CrossRefGoogle Scholar
  61. Kandel ER, Hudspeth AJ (2013) The brain and behavior. In: Kandel ER, Schwartz JH, Jessell TM et al (eds) Principles of neural science. McGraw-Hill, New York, pp 5–20Google Scholar
  62. Karmiloff-Smith A (1992) Beyond modularity: a developmental perspective on cognitive science. MIT Press, CambridgeGoogle Scholar
  63. Klein C (2010) Redeployed functions versus spreading activation: a potential confound. Behav Brain Sci 33(4):280–281CrossRefGoogle Scholar
  64. Klein C (2012) Cognitive ontology and region-versus network-oriented analyses. Philos Sci 79(5):952–960CrossRefGoogle Scholar
  65. Krubitzer L (1995) The organization of neocortex in mammals: are species differences really so different? Trends Neurosci 18(9):408–417CrossRefGoogle Scholar
  66. Laurence S, Margolis E (2015) Concept nativism and neural plasticity. In: Margolis E, Laurence S (eds) The conceptual mind: new directions in the study of concepts. MIT Press, Cambridge, pp 117–147Google Scholar
  67. Leise EM (1990) Modular construction of nervous systems: a basic principle of design for invertebrates and vertebrates. Brain Res Rev 15:1–23CrossRefGoogle Scholar
  68. MacNeilage PF (1998) The frame/content theory of evolution of speech production. Behav Brain Sci 21(4):499–511. discussion 511–546Google Scholar
  69. Maess B, Koelsch S, Gunter TC, Friederici AD (2001) Musical syntax is processed in Broca’s area: an MEG study. Nat Neurosci 4:540–545CrossRefGoogle Scholar
  70. Maleszka R, Mason PH, Barron AB (2013) Epigenomics and the concept of degeneracy in biological systems. Briefings Funct Genomics 13(3):191–202CrossRefGoogle Scholar
  71. Marr D (1976) Early processing of visual information. Philos Trans R Soc B 275:483–524CrossRefGoogle Scholar
  72. Martin A, Haxby JV, Lalonde FM, Wiggs CL, Ungerleider LG (1995) Discrete cortical regions associated with knowledge of color and knowledge of action. Sci 270:102–105CrossRefGoogle Scholar
  73. Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996) Neural correlates of category-specific knowledge. Nature 379(6566):649–652CrossRefGoogle Scholar
  74. Martin A, Ungerleider LG, Haxby JV (2000) Category-specificity and the brain: the sensorymotor model of semantic representations of objects. In: Gazzaniga MS (ed) The new cognitive neurosciences, 2nd edn. MIT Press, Cambridge, pp 1023–1036Google Scholar
  75. Mason PH (2010) Degeneracy at multiple levels of complexity. Biol Theory 5(3):277–288CrossRefGoogle Scholar
  76. Mather M, Cacioppo JT, Kanwisher N (2013) How fMRI can inform cognitive theories. Perspect Psychol Sci 8(1):108–113CrossRefGoogle Scholar
  77. Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20(4):408–434CrossRefGoogle Scholar
  78. Mountcastle VB (1978) An organizing principle for cerebral function: the unit module and the distributed system. In: Edelman G, Mountcastle VB (eds) The mindful brain. MIT Press, Cambridge, pp 7–50Google Scholar
  79. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722CrossRefGoogle Scholar
  80. Nishitani N, Schürmann M, Amunts K, Hari R (2005) Broca’s region: from action to language. Physiology 20:60–69CrossRefGoogle Scholar
  81. O’Reilly RC, Munakata Y, Frank MJ et al (2012) Computational cognitive neuroscience. 1st edn. Wiki Book.
  82. Ohlsson S (1994) Representational change, generality versus specificity, and nature versus nurture: perennial issues in cognitive research. Behav Brain Sci 17(4):724–725CrossRefGoogle Scholar
  83. Parfit D (1984) Reasons and persons. Oxford University Press, OxfordGoogle Scholar
  84. Pascual-Leone A, Hamilton R (2001) The metamodal organization of the brain. Prog Brain Res 134:427–445CrossRefGoogle Scholar
  85. Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401CrossRefGoogle Scholar
  86. Pasqualotto A (2016) Multisensory integration substantiates distributed and overlapping neural networks. Behav Brain Sci 39:20–21CrossRefGoogle Scholar
  87. Pessoa L (2016) Beyond disjoint brain networks: overlapping networks for cognition and emotion. Behav Brain Sci 39:22–24CrossRefGoogle Scholar
  88. Petrov AA, Jilk DJ, O’Reilly RC (2010) The Leabra architecture: specialization without modularity. Behav Brain Sci 33(4):286–287CrossRefGoogle Scholar
  89. Poldrack RA (2010) Mapping mental function to brain structure: how can cognitive neuroimaging succeed? Perspect Psychol Sci 5(6):753–761CrossRefGoogle Scholar
  90. Poldrack RA, Halchenko YO, Hanson SJ (2009) Decoding the large-scale structure of brain function by classifying mental states across individuals. Psychol Sci 20(11):1364–1372CrossRefGoogle Scholar
  91. Price CJ, Friston KJ (2005) Functional ontologies for cognition: the systematic definition of structure and function. Cogn Neuropsychol 22(3):262–275CrossRefGoogle Scholar
  92. Prinz JJ (2006) Is the mind really modular? In: Stainton R (ed) Contemporary debates in cognitive science. Blackwell, Oxford, pp 22–36Google Scholar
  93. Pulvermüller F (2005) Brain mechanisms linking language and action. Nat Rev Neurosci 6:576–582CrossRefGoogle Scholar
  94. Pulvermüller F, Fadiga L (2010) Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci 11:351–360CrossRefGoogle Scholar
  95. Rasmussen J (1986) Information processing and human-machine interaction. North-Holland, AmsterdamGoogle Scholar
  96. Rockland KS (2010) Five points on columns. Front Neuroanat 4(6):1–10Google Scholar
  97. Rowland DC, Moser MB (2014) From cortical modules to memories. Curr Opin Neurobiol 24:22–27CrossRefGoogle Scholar
  98. Sperber D (1994) The modularity of thought and the epidemiology of representations. In: Hirschfield LA, Gelman SA (eds) Mapping the mind. Cambridge University Press, Cambridge, pp 39–67CrossRefGoogle Scholar
  99. Sperber D (2002) In defense of massive modularity. In: Dupoux I (ed) Language, brain, and cognitive development. MIT Press, Cambridge, pp 47–57Google Scholar
  100. Sporns O (2015) Network neuroscience. In: Marcus G, Freeman J (eds) The future of the brain. Princeton University Press, Princeton, pp 90–99Google Scholar
  101. Stanton NA, Salmon PM (2009) Human error taxonomies applied to driving: a generic error taxonomy and its implications for intelligent transport systems. Saf Sci 47(2):227–237CrossRefGoogle Scholar
  102. Sternberg S (2011) Modular processes in mind and brain. Cogn Neuropsychol 28(3–4):156–208CrossRefGoogle Scholar
  103. Thoenissen D, Zilles K, Toni I (2002) Differential involvement of parietal and precentral regions in movement preparation and motor intention. J Neurosci 22:9024–9034CrossRefGoogle Scholar
  104. Walker GH, Stanton NA, Salmon PM (2015) Human factors in automotive engineering and technology. Ashgate, SurreyGoogle Scholar
  105. Wernicke C (1908) The symptom-complex of aphasia. In: Church A (ed) Diseases of the nervous system. Appleton, New York, pp 265–324Google Scholar
  106. Whiteacre JM (2010) Degeneracy: a link between evolvability, robustness and complexity in biological systems. Theor Biol Med Model 7(6):1–17Google Scholar
  107. Williams LE, Bargh JA (2008a) Experiencing physical warmth promotes interpersonal warmth. Science 322:606–607CrossRefGoogle Scholar
  108. Williams LE, Bargh JA (2008b) Keeping one’s distance: the influence of spatial distance cues on affect and evaluation. Psychol Sci 19:302–308CrossRefGoogle Scholar
  109. Zador A (2015) The connectome as a DNA sequencing problem. In: Marcus G, Freeman J (eds) The future of the brain. Princeton University Press, Princeton, pp 40–49Google Scholar
  110. Zerilli J (2017) Against the “system” module. Philos Psychol 30(3):235–250CrossRefGoogle Scholar
  111. Zerilli J (2019) Neural redundancy and its relation to neural reuse. Philos Sci (forthcoming)Google Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2018

Authors and Affiliations

  1. 1.Department of PhilosophyUniversity of OtagoDunedinNew Zealand

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