1932

Abstract

Categorization is our ability to flexibly assign sensory stimuli into discrete, behaviorally relevant groupings. Categorical decisions can be used to study decision making more generally by dissociating category identity of stimuli from the actions subjects use to signal their decisions. Here we discuss the evidence for such abstract categorical encoding in the primate brain and consider the relationship with other perceptual decision paradigms. Recent work on visual categorization has examined neuronal activity across a hierarchically organized network of cortical areas in monkeys trained to group visual stimuli into arbitrary categories. This has revealed a transformation of visual-feature encoding in early visual cortical areas into more flexible categorical representations in downstream parietal and prefrontal areas. These neuronal category representations are encoded as abstract internal cognitive states because they are not rigidly linked with either specific sensory stimuli or the actions that the monkeys use to signal their categorical choices.

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2016-07-08
2024-10-04
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Literature Cited

  1. Andersen RA. 1989. Visual and eye movement functions of the posterior parietal cortex. Annu. Rev. Neurosci. 12:377–403 [Google Scholar]
  2. Andersen RA, Snyder LH, Bradley DC, Xing J. 1997. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20:303–30 [Google Scholar]
  3. Antzoulatos EG, Miller EK. 2011. Differences between neural activity in prefrontal cortex and striatum during learning of novel abstract categories. Neuron 71:243–49 [Google Scholar]
  4. Ashby FG, Maddox WT. 2005. Human category learning. Annu. Rev. Psychol. 56:149–78 [Google Scholar]
  5. Ashby FG, Maddox WT. 2011. Human category learning 2.0. Ann. N.Y. Acad. Sci. 1224:147–61 [Google Scholar]
  6. Baldassi C, Alemi-Neissi A, Pagan M, Dicarlo JJ, Zecchina R, Zoccolan D. 2013. Shape similarity, better than semantic membership, accounts for the structure of visual object representations in a population of monkey inferotemporal neurons. PLOS Comput. Biol. 9:e1003167 [Google Scholar]
  7. Barsalou L. 1992. Cognitive Psychology: An Overview for Cognitive Scientists Hillsdale, NJ: Erlbaum [Google Scholar]
  8. Bennur S, Gold JI. 2011. Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J. Neurosci. 31:913–21 [Google Scholar]
  9. Bisley JW, Goldberg ME. 2010. Attention, intention, and priority in the parietal lobe. Annu. Rev. Neurosci. 33:1–21 [Google Scholar]
  10. Born RT, Bradley DC. 2005. Structure and function of visual area MT. Annu. Rev. Neurosci. 28:157–89 [Google Scholar]
  11. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA. 1996. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13:87–100 [Google Scholar]
  12. Cavada C, Goldman-Rakic PS. 1989. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287:422–45 [Google Scholar]
  13. Chafee MV, Goldman-Rakic PS. 1998. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J. Neurophysiol. 79:2919–40 [Google Scholar]
  14. Colby CL, Duhamel JR, Goldberg ME. 1996. Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J. Neurophysiol. 76:2841–52 [Google Scholar]
  15. Cromer JA, Roy JE, Buschman TJ, Miller EK. 2011. Comparison of primate prefrontal and premotor cortex neuronal activity during visual categorization. J. Cogn. Neurosci. 23:3355–65 [Google Scholar]
  16. Cromer JA, Roy JE, Miller EK. 2010. Representation of multiple, independent categories in the primate prefrontal cortex. Neuron 66:796–807 [Google Scholar]
  17. Crowe DA, Goodwin SJ, Blackman RK, Sakellaridi S, Sponheim SR. et al. 2013. Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition. Nat. Neurosci. 16:1484–91 [Google Scholar]
  18. Duffy CJ, Wurtz RH. 1991. Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J. Neurophysiol. 65:1329–45 [Google Scholar]
  19. Eiselt A-K, Nieder A. 2014. Rule activity related to spatial and numerical magnitudes: comparison of prefrontal, premotor, and cingulate motor cortices. J. Cogn. Neurosci. 26:1000–12 [Google Scholar]
  20. Engel TA, Chaisangmongkon W, Freedman DJ, Wang X-J. 2015. Choice-correlated activity fluctuations underlie learning of neuronal category representation. Nat. Commun. 6:6454 [Google Scholar]
  21. Eskandar EN, Assad JA. 1999. Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance. Nat. Neurosci. 2:88–93 [Google Scholar]
  22. Eskandar EN, Assad JA. 2002. Distinct nature of directional signals among parietal cortical areas during visual guidance. J. Neurophysiol. 88:1777–90 [Google Scholar]
  23. Fanini A, Assad JA. 2009. Direction selectivity of neurons in the macaque lateral intraparietal area. J. Neurophysiol. 101:289–305 [Google Scholar]
  24. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991 1:1–47 [Google Scholar]
  25. Ferrera VP, Grinband J. 2006. Walk the line: Parietal neurons respect category boundaries. Nat. Neurosci. 9:1207–8 [Google Scholar]
  26. Ferrera VP, Yanike M, Cassanello C. 2009. Frontal eye field neurons signal changes in decision criteria. Nat. Neurosci. 12:1458–62 [Google Scholar]
  27. Fitzgerald JK, Freedman DJ, Assad JA. 2011. Generalized associative representations in parietal cortex. Nat. Neurosci. 14:1075–79 [Google Scholar]
  28. Fitzgerald JK, Freedman DJ, Fanini A, Bennur S, Gold JI, Assad JA. 2013. Biased associative representations in parietal cortex. Neuron 77:180–91 [Google Scholar]
  29. Fitzgerald JK, Swaminathan SK, Freedman DJ. 2012. Visual categorization and the parietal cortex. Front. Integr. Neurosci. 6:18 [Google Scholar]
  30. Freedman DJ, Assad JA. 2006. Experience-dependent representation of visual categories in parietal cortex. Nature 443:85–88 [Google Scholar]
  31. Freedman DJ, Assad JA. 2009. Distinct encoding of spatial and nonspatial visual information in parietal cortex. J. Neurosci. 29:5671–80 [Google Scholar]
  32. Freedman DJ, Assad JA. 2011. A proposed common neural mechanism for categorization and perceptual decisions. Nat. Neurosci. 14:143–46 [Google Scholar]
  33. Freedman DJ, Miller EK. 2008. Neural mechanisms of visual categorization: insights from neurophysiology. Neurosci. Biobehav. Rev. 32:311–29 [Google Scholar]
  34. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. 2001. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291:312–16 [Google Scholar]
  35. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. 2002. Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. J. Neurophysiol. 88:929–41 [Google Scholar]
  36. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. 2003. A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J. Neurosci. 23:5235–46 [Google Scholar]
  37. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. 2006. Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. Cereb. Cortex 16:1631–44 [Google Scholar]
  38. Fuster JM, Bauer RH, Jervey JP. 1981. Effects of cooling inferotemporal cortex on performance of visual memory tasks. Exp. Neurol. 71:398–409 [Google Scholar]
  39. Fuster JM, Bauer RH, Jervey JP. 1982. Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Exp. Neurol. 77:679–94 [Google Scholar]
  40. Fuster JM, Jervey JP. 1981. Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. Science 212:952–55 [Google Scholar]
  41. Glimcher PW. 2003. Decisions, Uncertainty, and the Brain: The Science of Neuroeconomics Cambridge, MA: MIT Press [Google Scholar]
  42. Gnadt JW, Andersen RA. 1988. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70:216–20 [Google Scholar]
  43. Gold JI, Shadlen MN. 2007. The neural basis of decision making. Annu. Rev. Neurosci. 30:535–74 [Google Scholar]
  44. Goodwin SJ, Blackman RK, Sakellaridi S, Chafee MV. 2012. Executive control over cognition: stronger and earlier rule-based modulation of spatial category signals in prefrontal cortex relative to parietal cortex. J. Neurosci. 32:3499–515 [Google Scholar]
  45. Herrington TM, Assad JA. 2009. Neural activity in the middle temporal area and lateral intraparietal area during endogenously cued shifts of attention. J. Neurosci. 29:14160–76 [Google Scholar]
  46. Herrington TM, Assad JA. 2010. Temporal sequence of attentional modulation in the lateral intraparietal area and middle temporal area during rapid covert shifts of attention. J. Neurosci. 30:3287–96 [Google Scholar]
  47. Hubel DH, Wiesel TN. 1959. Receptive fields of single neurones in the cat's striate cortex. J. Physiol. 148:574–91 [Google Scholar]
  48. Hubel DH, Wiesel TN. 1968. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:215–43 [Google Scholar]
  49. Ibos G, Freedman DJ. 2014. Dynamic integration of task-relevant visual features in posterior parietal cortex. Neuron 83:1468–80 [Google Scholar]
  50. Kiani R, Shadlen MN. 2009. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 324:759–64 [Google Scholar]
  51. Kourtzi Z, Connor CE. 2011. Neural representations for object perception: structure, category, and adaptive coding. Annu. Rev. Neurosci. 34:45–67 [Google Scholar]
  52. Kriegeskorte N, Mur M, Ruff DA, Kiani R, Bodurka J. et al. 2008. Matching categorical object representations in inferior temporal cortex of man and monkey. Neuron 60:1126–41 [Google Scholar]
  53. Leathers ML, Olson CR. 2012. In monkeys making value-based decisions, LIP neurons encode cue salience and not action value. Science 338:132–35 [Google Scholar]
  54. Leathers ML, Olson CR. 2013. Response to comment on “In monkeys making value-based decisions, LIP neurons encode cue salience and not action value.”. Science 340:430 [Google Scholar]
  55. 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. 428:112–37 [Google Scholar]
  56. Liu N, Kriegeskorte N, Mur M, Hadj-Bouziane F, Luh W-M. et al. 2013. Intrinsic structure of visual exemplar and category representations in macaque brain. J. Neurosci. 33:11346–60 [Google Scholar]
  57. Logothetis NK, Sheinberg DL. 1996. Visual object recognition. Annu. Rev. Neurosci. 19:577–621 [Google Scholar]
  58. Long B, Konkle T, Cohen MA, Alvarez GA. 2016. Mid-level perceptual features distinguish objects of different real-world sizes. J. Exp. Psychol. Gen. 145:95–109 [Google Scholar]
  59. Maimon G, Assad JA. 2006a. A cognitive signal for the proactive timing of action in macaque LIP. Nat. Neurosci. 9:948–55 [Google Scholar]
  60. Maimon G, Assad JA. 2006b. Parietal area 5 and the initiation of self-timed movements versus simple reactions. J. Neurosci. 26:2487–98 [Google Scholar]
  61. Maunsell JHR. 2004. Neuronal representations of cognitive state: reward or attention?. Trends Cogn. Sci. 8:261–65 [Google Scholar]
  62. McKee JL, Riesenhuber M, Miller EK, Freedman DJ. 2014. Task dependence of visual and category representations in prefrontal and inferior temporal cortices. J. Neurosci. 34:16065–75 [Google Scholar]
  63. Meister MLR, Hennig JA, Huk AC. 2013. Signal multiplexing and single-neuron computations in lateral intraparietal area during decision-making. J. Neurosci. 33:2254–67 [Google Scholar]
  64. Miller EK, Cohen JD. 2001. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24:167–202 [Google Scholar]
  65. Movshon JA, Adelson EH, Gizzi MS, Newsome WT. 1986. The analysis of moving visual patterns. Exp. Brain Res. Suppl. 11:117–51 [Google Scholar]
  66. Muhammad R, Wallis JD, Miller EK. 2006. A comparison of abstract rules in the prefrontal cortex, premotor cortex, inferior temporal cortex, and striatum. J. Cogn. Neurosci. 18:974–89 [Google Scholar]
  67. Newsome WT, Britten KH, Movshon JA. 1989. Neuronal correlates of a perceptual decision. Nature 341:52–54 [Google Scholar]
  68. Nieder A, Diester I, Tudusciuc O. 2006. Temporal and spatial enumeration processes in the primate parietal cortex. Science 313:1431–35 [Google Scholar]
  69. Nieder A, Freedman DJ, Miller EK. 2002. Representation of the quantity of visual items in the primate prefrontal cortex. Science 297:1708–11 [Google Scholar]
  70. Nieder A, Miller EK. 2004. A parieto-frontal network for visual numerical information in the monkey. PNAS 101:7457–62 [Google Scholar]
  71. Oristaglio J, Schneider DM, Balan PF, Gottlieb J. 2006. Integration of visuospatial and effector information during symbolically cued limb movements in monkey lateral intraparietal area. J. Neurosci. 26:8310–19 [Google Scholar]
  72. Padoa-Schioppa C. 2011. Neurobiology of economic choice: a good-based model. Annu. Rev. Neurosci. 34:333–59 [Google Scholar]
  73. Padoa-Schioppa C, Assad JA. 2006. Neurons in the orbitofrontal cortex encode economic value. Nature 441:223–26 [Google Scholar]
  74. Parker AJ, Newsome WT. 1998. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21:227–77 [Google Scholar]
  75. Petrides M, Pandya DN. 1984. Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J. Comp. Neurol. 228:105–16 [Google Scholar]
  76. Rishel CA, Huang G, Freedman DJ. 2013. Independent category and spatial encoding in parietal cortex. Neuron 77:969–79 [Google Scholar]
  77. Roy JE, Buschman TJ, Miller EK. 2014. PFC neurons reflect categorical decisions about ambiguous stimuli. J. Cogn. Neurosci. 26:1283–91 [Google Scholar]
  78. Saito H, Yukie M, Tanaka K, Hikosaka K, Fukada Y, Iwai E. 1986. Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. J. Neurosci. 6:145–57 [Google Scholar]
  79. Sarma A, Masse NY, Wang X-J, Freedman DJ. 2016. Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices. Nat. Neurosci. 19:143–49 [Google Scholar]
  80. Seger CA, Miller EK. 2010. Category learning in the brain. Annu. Rev. Neurosci. 33:203–19 [Google Scholar]
  81. Sereno AB, Maunsell JHR. 1998. Shape selectivity in primate lateral intraparietal cortex. Nature 395:500–3 [Google Scholar]
  82. Shadlen MN, Kiani R. 2013. Decision making as a window on cognition. Neuron 80:791–806 [Google Scholar]
  83. Shadlen MN, Kiani R, Hanks TD, Churchland AK. 2008. Neurobiology of decision making: an intentional framework. Better Than Conscious? Decision Making, the Human Mind, and Implications for Institutions C Engel, W Singer 71–102 Cambridge, MA: MIT Press [Google Scholar]
  84. Shadlen MN, Newsome WT. 2001. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86:1916–36 [Google Scholar]
  85. Snyder LH, Batista AP, Andersen RA. 1997. Coding of intention in the posterior parietal cortex. Nature 386:167–70 [Google Scholar]
  86. Squire RF, Noudoost B, Schafer RJ, Moore T. 2013. Prefrontal contributions to visual selective attention. Annu. Rev. Neurosci. 36:451–66 [Google Scholar]
  87. Stoet G, Snyder LH. 2004. Single neurons in posterior parietal cortex of monkeys encode cognitive set. Neuron 42:1003–12 [Google Scholar]
  88. Swaminathan SK, Freedman DJ. 2012. Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex. Nat. Neurosci. 15:315–20 [Google Scholar]
  89. Swaminathan SK, Masse NY, Freedman DJ. 2013. A comparison of lateral and medial intraparietal areas during a visual categorization task. J. Neurosci. 33:13157–70 [Google Scholar]
  90. Tanaka K. 1996. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19:109–39 [Google Scholar]
  91. Tsao DY, Livingstone MS. 2008. Mechanisms of face perception. Annu. Rev. Neurosci. 31:411–37 [Google Scholar]
  92. Tudusciuc O, Nieder A. 2007. Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex. PNAS 104:14513–18 [Google Scholar]
  93. Vallentin D, Bongard S, Nieder A. 2012. Numerical rule coding in the prefrontal, premotor, and posterior parietal cortices of macaques. J. Neurosci. 32:6621–30 [Google Scholar]
  94. Vogels R. 1999a. Categorization of complex visual images by rhesus monkeys. Part 1: behavioural study. Eur. J. Neurosci. 11:1223–38 [Google Scholar]
  95. Vogels R. 1999b. Categorization of complex visual images by rhesus monkeys. Part 2: single-cell study. Eur. J. Neurosci. 11:1239–55 [Google Scholar]
  96. Wallis JD. 2007. Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30:31–56 [Google Scholar]
  97. Wallis JD, Anderson KC, Miller EK. 2001. Single neurons in prefrontal cortex encode abstract rules. Nature 411:953–56 [Google Scholar]
  98. Wallis JD, Miller EK. 2003. From rule to response: neuronal processes in the premotor and prefrontal cortex. J. Neurophysiol. 90:1790–806 [Google Scholar]
  99. Williams ZM, Elfar JC, Eskandar EN, Toth LJ, Assad JA. 2003. Parietal activity and the perceived direction of ambiguous apparent motion. Nat. Neurosci. 6:616–23 [Google Scholar]
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