Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A unified model of human semantic knowledge and its disorders

Abstract

How is knowledge about the meanings of words and objects represented in the human brain? Current theories embrace two radically different proposals: either distinct cortical systems have evolved to represent different kinds of things, or knowledge for all kinds is encoded within a single domain-general network. Neither view explains the full scope of relevant evidence from neuroimaging and neuropsychology. Here we propose that graded category-specificity emerges in some components of the semantic network through joint effects of learning and network connectivity. We test the proposal by measuring connectivity amongst cortical regions implicated in semantic representation, then simulating healthy and disordered semantic processing in a deep neural network whose architecture mirrors this structure. The resulting neuro-computational model explains the full complement of neuroimaging and patient evidence adduced in support of both domain-specific and domain-general approaches, reconciling long-standing disputes about the nature and origins of this uniquely human cognitive faculty.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: ALE analysis showing regions that systematically respond more to animals than artifacts (orange), more to artifacts than animals (blue), or equally to both (green).
Figure 2: Tractography results.
Figure 3: Model architecture and functional magnetic resonance imaging (fMRI) data simulations.
Figure 4: Results of patient simulations.

References

  1. 1

    Fernandino, L. et al. Predicting brain activation patterns associated with individual lexical concepts based on five sensory-motor attributes. Neuropsychologia 76, 17–26 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  2. 2

    Caramazza, A. & Shelton, J. R. Domain-specific knowledge systems in the brain: the animate–inanimate distinction. J. Cogn. Neurosci. 10, 1–34 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. 3

    Caramazza, A. & Mahon, B. Z. The organization of conceptual knowledge: the evidence from category-specific semantic deficits. Trends Cogn. Sci. 7, 354–361 (2003).

    PubMed  Article  PubMed Central  Google Scholar 

  4. 4

    Patterson, K., Nestor, P. J. & Rogers, T. T. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat. Rev. Neurosci 8, 976–987 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  5. 5

    Rogers, T. T. et al. The structure and deterioration of semantic memory: a computational and neuropsychological investigation. Psychol. Rev. 111, 205–235 (2004).

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6

    Tyler, L. K., Moss, H. E., Durrant-Peatfield, M. R. & Levy, J. P. Conceptual structure and the structure of concepts: a distributed account of category-specific deficits. Brain Lang. 75, 195–231 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. 7

    Chen, L. & Rogers, T. T. Revisiting domain-general accounts of category specificity in mind and brain. Wiley Interdiscip. Rev. Cogn. Sci. 5, 327–44 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  8. 8

    Plaut, D. C. Graded modality-specific specialisation in semantics: a computational account of optic aphasia. Cogn. Neuropsychol. 19, 603–639 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  9. 9

    Mahon, B. Z., Anzellotti, S., Schwarzbach, J., Zampini, M. & Caramazza, A. Category-specific organization in the human brain does not require visual experience. Neuron 63, 397–405 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10

    Warrington, E. K. & Shallice, T. Category specific semantic impairments. Brain 107, 829–854 (1984).

    Article  Google Scholar 

  11. 11

    Cree, G. S. & McRae, K. Analyzing the factors underlying the structure and computation of the meaning of chipmunk, cherry, chisel, cheese, and cello (and many other such concrete nouns). J. Exp. Psychol. Gen. 132, 163–201 (2003).

    PubMed  Article  Google Scholar 

  12. 12

    Chen, L. & Rogers, T. T. A model of emergent category-specific activation in the posterior fusiform gyrus of sighted and congenitally blind populations. J. Cogn. Neurosci. 27, 1981–1999 (2015).

    PubMed  Article  Google Scholar 

  13. 13

    Pobric, G., Jefferies, E. & Lambon Ralph, M. A. Category-specific versus category-general semantic impairment induced by transcranial magnetic stimulation. Curr. Biol. 20, 964–968 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. 14

    Sadtler, P. T. et al. Neural constraints on learning. Nature 512, 423–426 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15

    Gomez, J. et al. Functionally defined white matter reveals segregated pathways in human ventral temporal cortex associated with category-specific processing. Neuron 85, 216–227 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16

    Mahon, B. Z. & Caramazza, A. What drives the organization of object knowledge in the brain? Trends Cogn. Sci. 15, 97–103 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17

    Plaut, D. C. & Behrmann, M. Complementary neural representations for faces and words: a computational exploration. Cogn. Neuropsychol. 28, 251–275 (2011).

    PubMed  Article  Google Scholar 

  18. 18

    Martin, A. & Chao, L. L. Semantic memory and the brain: structure and processes. Curr. Opin. Neurobiol. 11, 194–201 (2001).

    CAS  PubMed  Article  Google Scholar 

  19. 19

    Mahon, B. Z. et al. Action-related properties shape object representations in the ventral stream. Neuron 55, 507–520 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20

    Hickok, G. & Poeppel, D. The cortical organization of speech processing. Nat. Rev. Neurosci. 8, 393–402 (2007).

    CAS  PubMed  Article  Google Scholar 

  21. 21

    Kellenbach, M. L., Brett, M. & Patterson, K. Actions speak louder than functions: the importance of manipulability and action in tool representation. J. Cogn. Neurosci. 15, 30–46 (2003).

    PubMed  Article  Google Scholar 

  22. 22

    Chouinard, P. A & Goodale, M. A. Category-specific neural processing for naming pictures of animals and naming pictures of tools: an ALE meta-analysis. Neuropsychologia 48, 409–418 (2010).

    PubMed  Article  Google Scholar 

  23. 23

    Pobric, G., Jefferies, E. & Lambon Ralph, M. A. Anterior temporal lobes mediate semantic representation: mimicking semantic dementia by using rTMS in normal participants. Proc. Natl Acad. Sci. USA 104, 20137–20141 (2007).

    CAS  PubMed  Article  Google Scholar 

  24. 24

    Acosta-Cabronero, J. et al. Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. Brain 134, 2025–2035 (2011).

    PubMed  Article  Google Scholar 

  25. 25

    Chouinard, P. A. & Goodale, M. A. Category-specific neural processing for naming pictures of animals and naming pictures of tools: an ALE meta-analysis. Neuropsychologia 48, 409 (2010).

    PubMed  Article  Google Scholar 

  26. 26

    Hwang, K. et al. Category-specific activations during word generation reflect experiential sensorimotor modalities. Neuroimage 48, 717–725 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  27. 27

    Smith, C. D. et al. Differences in functional magnetic resonance imaging activation by category in a visual confrontation naming task. J. Neuroimaging 11, 165–170 (2001).

    CAS  PubMed  Article  Google Scholar 

  28. 28

    Grossman, M. et al. The neural basis for category-specific knowledge: an fMRI study. Neuroimage 15, 936–948 (2002).

    PubMed  Article  Google Scholar 

  29. 29

    Martin, A., Haxby, J. V, Lalonde, F. M., Wiggs, C. L. & Ungerleider, L. G. Discrete cortical regions associated with knowledge of color and knowledge of action. Science 270, 102–105 (1995).

    CAS  PubMed  Article  Google Scholar 

  30. 30

    Tyler, L. K. et al. Do semantic categories activate distinct cortical regions? Evidence for a distributed neural semantic system. Cogn. Neuropsychol. 20, 541–559 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. 31

    Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D. & Damasio, A. R. A neural basis for lexical retrieval. Nature 380, 499–505 (1996).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. 32

    Cappa, S. F., Perani, D., Schnur, T., Tettamanti, M. & Fazio, F. The effects of semantic category and knowledge type on lexical-semantic access: a PET study. Neuroimage 8, 350–359 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. 33

    Mechelli, A., Sartori, G., Orlandi, P. & Price, C. J. Semantic relevance explains category effects in medial fusiform gyri. Neuroimage 30, 992–1002 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34

    Noppeney, U., Josephs, O., Kiebel, S., Friston, K. J. & Price, C. J. Action selectivity in parietal and temporal cortex. Brain Res. Cogn. Brain Res. 25, 641 (2005).

    CAS  PubMed  Article  Google Scholar 

  35. 35

    Phillips, J. A., Noppeney, U., Humphreys, G. W. & Price, C. J. Can segregation within the semantic system account for category-specific deficits? Brain 125, 2067–2080 (2002).

    PubMed  Article  Google Scholar 

  36. 36

    Kroliczak, G. & Frey, S. H. A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cereb. Cortex 19, 2396–2410 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  37. 37

    Grossman, M. et al. Category-specific semantic memory: converging evidence from bold fMRI and Alzheimer’s disease. Neuroimage 68, 263–274 (2013).

    PubMed  Article  Google Scholar 

  38. 38

    Laine, M., Rinne, J. O., Hiltunen, J., Kaasinen, V. & Sipilä, H. Different brain activation patterns during production of animals versus artefacts: a PET activation study on category-specific processing. Cogn. Brain Res. 13, 95–99 (2002).

    Article  Google Scholar 

  39. 39

    Boronat, C. B. et al. Distinctions between manipulation and function knowledge of objects: evidence from functional magnetic resonance imaging. Cogn. Brain Res. 23, 361–373 (2005).

    Article  Google Scholar 

  40. 40

    Gorno-Tempini, M.-L. Category differences in brain activation studies: where do they come from? Proc. R. Soc. Lond. B 267, 1253–1258 (2000).

    CAS  Article  Google Scholar 

  41. 41

    Gerlach, C., Law, I. & Paulson, O. B. When action turns into words. Activation of motor-based knowledge during categorization of manipulable objects. J. Cogn. Neurosci. 14, 1230–1239 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  42. 42

    Rogers, T. T., Hocking, J., Mechelli, A., Patterson, K. & Price, C. Fusiform activation to animals is driven by the process, not the stimulus. J. Cogn. Neurosci. 17, 434–445 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  43. 43

    Lewis, J. W., Brefczynski, J. A., Phinney, R. E., Janik, J. J. & DeYoe, E. A. Distinct cortical pathways for processing tool versus animal sounds. J. Neurosci. 25, 5148–5158 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. 44

    Canessa, N. et al. The different neural correlates of action and functional knowledge in semantic memory: an fMRI study. Cereb. Cortex 18, 740–751 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  45. 45

    Joseph, J. E., Gathers, A. D. & Piper, G. A. Shared and dissociated cortical regions for object and letter processing. Cogn. Brain Res. 17, 56–67 (2003).

    Article  Google Scholar 

  46. 46

    Gerlach, C. et al. Brain activity related to integrative processes in visual object recognition: bottom-up integration and the modulatory influence of stored knowledge. Neuropsychologia 40, 1254–1267 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  47. 47

    Gerlach, C., Law, I., Gade, A. & Paulson, O. B. Categorization and category effects in normal object recognition: a PET study. Neuropsychologia 38, 1693–1703 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  48. 48

    Devlin, J. T., Rushworth, M. F. S. & Matthews, P. M. Category-related activation for written words in the posterior fusiform is task specific. Neuropsychologia 43, 69–74 (2005).

    PubMed  PubMed Central  Article  Google Scholar 

  49. 49

    Noppeney, U., Price, C. J., Penny, W. D. & Friston, K. J. Two distinct neural mechanisms for category-selective responses. Cereb. Cortex 16, 437–445 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  50. 50

    Whatmough, C., Chertkow, H., Murtha, S. & Hanratty, K. Dissociable brain regions process object meaning and object structure during picture naming. Neuropsychologia 40, 174–186 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. 51

    Grafton, S. T., Fadiga, L., Arbib, M. A. & Rizzolatti, G. Premotor cortex activation during observation and naming of familiar tools. Neuroimage 6, 231–236 (1997).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. 52

    Chao, L. L., Haxby, J. V. & Martin, A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat. Neurosci. 2, 913–919 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  53. 53

    Chao, L. L. & Martin, A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478–484 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54

    Goldberg, R. F., Perfetti, C. A. & Schneider, W. Perceptual knowledge retrieval activates sensory brain regions. J. Neurosci. 26, 4917–4921 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. 55

    Bai, H. M. et al. Functional MRI mapping of category-specific sites associated with naming of famous faces, animals and man-made objects. Neurosci. Bull. 27, 307–318 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  56. 56

    Folstein, J. R., Palmeri, T. J. & Gauthier, I. Category learning increases discriminability of relevant object dimensions in visual cortex. Cereb. Cortex 23, 814–823 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  57. 57

    Martin, A, Wiggs, C. L., Ungerleider, L. G. & Haxby, J. V. Neural correlates of category-specific knowledge. Nature 379, 649–652 (1996).

    CAS  Article  Google Scholar 

  58. 58

    Perani, D. et al. Word and picture matching: a PET study of semantic category effects. Neuropsychologia 37, 293–306 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  59. 59

    Handy, T. C., Grafton, S. T., Shroff, N. M., Ketay, S. & Gazzaniga, M. S. Graspable objects grab attention when the potential for action is recognized. Nat. Neurosci. 6, 421–427 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  60. 60

    Gerlach, C., Law, I. & Paulson, O. B. Structural similarity and category-specificity: a refined account. Neuropsychologia 42, 1543–1553 (2004).

    PubMed  Article  PubMed Central  Google Scholar 

  61. 61

    Wadsworth, H. M. & Kana, R. K. Brain mechanisms of perceiving tools and imagining tool use acts: a functional MRI study. Neuropsychologia 49, 1863–1869 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  62. 62

    Okada, T. et al. Naming of animals and tools: a functional magnetic resonance imaging study of categorical differences in the human brain areas commonly used for naming visually presented objects. Neurosci. Lett. 296, 33 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  63. 63

    Mahon, B. Z., Schwarzbach, J. & Caramazza, A. The representation of tools in left parietal cortex is independent of visual experience. Psychol. Sci. 21, 764–771 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  64. 64

    Creem-Regehr, S. H. & Lee, J. N. Neural representations of graspable objects: are tools special? Cogn. Brain Res. 22, 457–469 (2005).

    Article  Google Scholar 

  65. 65

    Mruczek, R. E. B., von Loga, I. S. & Kastner, S. The representation of tool and non-tool object information in the human intraparietal sulcus. J. Neurophysiol. 109, 2883–2896 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  66. 66

    Zannino, G. D. et al. Visual and semantic processing of living things and artifacts: an fMRI study. J. Cogn. Neurosci. 22, 554–570 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  67. 67

    Chao, L. L., Weisberg, J. & Martin, A. Experience-dependent modulation of category-related cortical activity. Cereb. Cortex 12, 545–551 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  68. 68

    Anzellotti, S., Mahon, B. Z., Schwarzbach, J. & Caramazza, A. Differential activity for animals and manipulable objects in the anterior temporal lobes. J. Cogn. Neurosci. 23, 2059–2067 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  69. 69

    Moore, C. J. & Price, C. J. A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain 122, 943–962 (1999).

    PubMed  Article  PubMed Central  Google Scholar 

  70. 70

    Tranel, D., Martin, C., Damasio, H., Grabowski, T. J. & Hichwa, R. Effects of noun–verb homonymy on the neural correlates of naming concrete entities and actions. Brain Lang. 92, 288–299 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  71. 71

    Grabowski, T. J., Damasio, H. & Damasio, A. R. Premotor and prefrontal correlates of category-related lexical retrieval. Neuroimage 7, 232–243 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. 72

    Eickhoff, S. B., Bzdok, D., Laird, A. R., Kurth, F. & Fox, P. T. Activation likelihood estimation meta-analysis revisited. Neuroimage 59, 2349–2361 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  73. 73

    Martin, A. The representation of object concepts in the brain. Annu. Rev. Psychol. 58, 25–45 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  74. 74

    Ueno, T., Saito, S., Rogers, T. T. & Lambon Ralph, M. A. Lichtheim 2: synthesizing aphasia and the neural basis of language in a neurocomputational model of the dual dorsal-ventral language pathways. Neuron 72, 385–96 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  75. 75

    Visser, M., Jefferies, E. & Lambon Ralph, M. A. Semantic processing in the anterior temporal lobes: a meta-analysis of the functional neuroimaging literature. J. Cogn. Neurosci. 22, 1083–1094 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  76. 76

    Adlam, A. L. R. et al. Semantic dementia and fluent primary progressive aphasia: two sides of the same coin? Brain 129, 3066–3080 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  77. 77

    Shimotake, A. et al. Direct exploration of the role of the ventral anterior temporal lobe in semantic memory: cortical stimulation and local field potential evidence from subdural grid electrodes. Cereb. Cortex 25, 3802–3817 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  78. 78

    Lambon Ralph, M. A., Lowe, C. & Rogers, T. T. Neural basis of category-specific semantic deficits for living things: evidence from semantic dementia, HSVE and a neural network model. Brain 130, 1127–1137 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  79. 79

    Binkofski, F. & Buxbaum, L. J. Two action systems in the human brain. Brain Lang. 127, 222–229 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  80. 80

    Humphreys, G. W. & Riddoch, M. J. Features, objects, action: the cognitive neuropsychology of visual object processing, 1984–2004. Cogn. Neuropsychol. 23, 156–183 (2006).

    PubMed  Article  Google Scholar 

  81. 81

    Humphreys, G. F. & Lambon Ralph, M. A. Fusion and fission of cognitive functions in the human parietal cortex. Cereb. Cortex 25, 3547–3560 (2015).

    PubMed  Article  Google Scholar 

  82. 82

    Jung, J., Cloutman, L. L., Binney, R. J. & Ralph, M. A. L. The structural connectivity of higher order association cortices reflects human functional brain networks. Cortex http://dx.doi.org/10.1016/j.cortex.2016.08.011 (2016).

  83. 83

    Embleton, K. V., Haroon, H. A., Morris, D. M., Lambon Ralph, M. A. & Parker, G. J. M. Distortion correction for diffusion-weighted MRI tractography and fMRI in the temporal lobes. Hum. Brain Mapp. 31, 1570–1587 (2010).

    PubMed  Article  Google Scholar 

  84. 84

    Binney, R. J., Embleton, K. V, Jefferies, E., Parker, G. J. M. & Lambon Ralph, M. A. The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. Cereb. Cortex 20, 2728–2738 (2010).

    PubMed  Article  Google Scholar 

  85. 85

    Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G. & Mishkin, M. The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 17, 26–49 (2013).

    PubMed  Article  Google Scholar 

  86. 86

    Binney, R. J., Parker, G. J. M. & Lambon Ralph, M. A. Convergent connectivity and graded specialization in the rostral human temporal lobe as revealed by diffusion-weighted imaging probabilistic tractography. J. Cogn. Neurosci. 24, 1998–2014 (2012).

    PubMed  Article  Google Scholar 

  87. 87

    Schmahmann, J. D. & Pandya, D. Fiber Pathways of the Brain (Oxford Univ. Press, 2009).

    Google Scholar 

  88. 88

    Bajada, C. J., Lambon Ralph, M. A. & Cloutman, L. L. Transport for language south of the Sylvian fissure: the routes and history of the main tracts and stations in the ventral language network. Cortex 69, 141–151 (2015).

    PubMed  Article  Google Scholar 

  89. 89

    Bedny, M., Caramazza, A., Pascual-Leone, A. & Saxe, R. Typical neural representations of action verbs develop without vision. Cereb. Cortex 22, 286–293 (2012).

    CAS  PubMed  Article  Google Scholar 

  90. 90

    Warrington, E. K. & McCarthy, R. Category specific access dysphasia. Brain 106, 859–878 (1983).

    PubMed  Article  Google Scholar 

  91. 91

    Gotts, S. & Plaut, D. C. The impact of synaptic depression following brain damage: a connectionist account of ‘access/refractory’ and ‘degraded-store’ semantic impairments. Cogn. Affect. Behav. Neurosci. 2, 187–213 (2002).

    PubMed  Article  Google Scholar 

  92. 92

    Noppeney, U. et al. Temporal lobe lesions and semantic impairment: a comparison of herpes simplex virus encephalitis and semantic dementia. Brain 130, 1138–1147 (2007).

    PubMed  Article  Google Scholar 

  93. 93

    Campanella, F., D’Agostini, S., Skrap, M. & Shallice, T. Naming manipulable objects: anatomy of a category specific effect in left temporal tumours. Neuropsychologia 48, 1583–1597 (2010).

    PubMed  Article  Google Scholar 

  94. 94

    Roberts, D. Exploring the Link Between Visual Impairment and Pure Alexia. PhD thesis, Univ. Manchester (2009).

    Google Scholar 

  95. 95

    Humphreys, G. W. & Forde, E. M. E. Category specificity in mind and brain? Behav. Brain Sci. 24, 497–509 (2001).

    Google Scholar 

  96. 96

    Laiacona, M., Capitani, E. & Barbarotto, R. Semantic category dissociations: a longitudinal study of two cases. Cortex 33, 441–461 (1997).

    CAS  PubMed  Article  Google Scholar 

  97. 97

    Pietrini, V. et al. Recovery from herpes simplex encephalitis: selective impairment of specific semantic categories with neuroradiological correlation. J. Neurol. Neurosurg. Psychiatry 51, 1284–1293 (1988).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. 98

    Damasio, H., Tranel, D., Grabowski, T., Adolphs, R. & Damasio, A. Neural systems behind word and concept retrieval. Cognition 92, 179–229 (2004).

    CAS  PubMed  Article  Google Scholar 

  99. 99

    Plaut, D. C. & Behrmann, M. Complementary neural representations for faces and words: a computational exploration. Cogn. Neuropsychol. 28, 251–275 (2011).

    PubMed  Article  Google Scholar 

  100. 100

    Farah, M. J. & McClelland, J. L. A computational model of semantic memory impairment: modality-specificity and emergent category-specificity. J. Exp. Psychol. Gen. 120, 339–357 (1991).

    CAS  PubMed  Article  Google Scholar 

  101. 101

    Badre, D. & Wagner, A. Semantic retrieval, mnemonic control, and prefrontal cortex. Behav. Cogn. Neurosci. Rev. 1, 206–218 (2002).

    PubMed  Article  Google Scholar 

  102. 102

    LeCun, Y., Bengio, Y. & Hinton, G. Deep learning. Nature 521, 436–444 (2015).

    CAS  Article  Google Scholar 

  103. 103

    McClelland, J. L., Rumelhart, D. E. & Hinton, G. E. in Parallel Distributed Processing: Explorations in the Microstructure of Cognition Vol. 1 (eds Rumelhart, D. E., McClelland, J. L. & the PDP Research Group ) 3–44 (MIT Press, 1986).

    Google Scholar 

  104. 104

    Price, C. J., Devlin, J. T., Moore, C. J., Morton, C. & Laird, A. R. Meta-analyses of object naming: effect of baseline. Hum. Brain Mapp. 25, 70–82 (2005).

    PubMed  Article  Google Scholar 

  105. 105

    Turkeltaub, P. E. et al. Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum. Brain Mapp. 33, 1–13 (2012).

    PubMed  Article  Google Scholar 

  106. 106

    Oldfield, R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).

    CAS  PubMed  Article  Google Scholar 

  107. 107

    Eickhoff, S. B. et al. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 30, 2907–2926 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  108. 108

    Cloutman, L. L., Binney, R. J., Drakesmith, M., Parker, G. J. M. & Lambon Ralph, M. A. The variation of function across the human insula mirrors its patterns of structural connectivity: evidence from in vivo probabilistic tractography. Neuroimage 59, 3514–3521 (2012).

    PubMed  Article  Google Scholar 

  109. 109

    Visser, M. & Lambon Ralph, M. A. Differential contributions of bilateral ventral anterior temporal lobe and left anterior superior temporal gyrus to semantic processes. J. Cogn. Neurosci. 23, 3121–3131 (2011).

    CAS  PubMed  Article  Google Scholar 

  110. 110

    Pobric, G., Jefferies, E. & Lambon Ralph, M. A. Category-specific versus category-general semantic impairment induced by transcranial magnetic stimulation. Curr. Biol. 20, 964–968 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. 111

    Parker, G. J. M. & Alexander, D. C. Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue. Phil. Trans. R. Soc. B 360, 893–902 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  112. 112

    Rohde, D. L. T. LENS: The Light, Efficient Network Simulator. Technical Report CMU-CS-99-164 (Carnegie Mellon Univ., 1999).

  113. 113

    Rumelhart, D. E., Hinton, G. E. & Williams, R. J. Learning Representations by Back-Propagating Errors (MIT Press, 1988).

    Google Scholar 

  114. 114

    Garrard, P. & Carroll, E. Lost in semantic space: a multi-modal, non-verbal assessment of feature knowledge in semantic dementia. Brain 129, 1152–1163 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  115. 115

    Dixon, M. J., Bub, D. N. & Arguin, M. The interaction of object form and object meaning in the identification performance of a patient with category-specific visual agnosia. Cogn. Neuropsychol. 14, 1085–1130 (1997).

    Article  Google Scholar 

  116. 116

    Dixon, M. J., Bub, D. N., Chertkow, H. & Arguin, M. Object identification deficits in dementia of the Alzheimer type: combined effects of semantic and visual proximity. J. Int. Neuropsychol. Soc. 5, 330–345 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  117. 117

    Zevin, J. D. & Seidenberg, M. S. Simulating consistency effects and individual differences in nonword naming: a comparison of current models. J. Mem. Lang. 54, 145–160 (2006).

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by a programme grant from the Medical Research Council (MRC, UK, MR/J004146/1) to M.A.L.R. and by a University Fellowship from UW-Madison to L.C. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank L. Cloutman for assisting with the tractography analysis and R. Ishibashi for assisting with the ALE analysis.

Author information

Affiliations

Authors

Contributions

All authors contributed to the entire process of this project, including project planning, experiment work, data analysis and writing the paper.

Corresponding authors

Correspondence to Lang Chen, Matthew A. Lambon Ralph or Timothy T. Rogers.

Ethics declarations

Competing interests

The authors declare no competing interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–8, Supplementary tables 1–7, Supplementary Discussion, Supplementary Methods, Supplementary References (PDF 3425 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, L., Lambon Ralph, M. & Rogers, T. A unified model of human semantic knowledge and its disorders. Nat Hum Behav 1, 0039 (2017). https://doi.org/10.1038/s41562-016-0039

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing