Perirhinal circuits for memory processing

Abstract

The perirhinal cortex (PRC) serves as the gateway to the hippocampus for episodic memory formation and plays a part in retrieval through its backward connectivity to various neocortical areas. First, I present the evidence suggesting that PRC neurons encode both experientially acquired object features and their associative relations. Recent studies have revealed circuit mechanisms in the PRC for the retrieval of cue-associated information, and have demonstrated that, in monkeys, PRC neuron-encoded information can be behaviourally read out. These studies, among others, support the theory that the PRC converts visual representations of an object into those of its associated features and initiates backward-propagating, interareal signalling for retrieval of nested associations of object features that, combined, extensionally represent the object meaning. I propose that the PRC works as the ventromedial hub of a ‘two-hub model’ at an apex of the hierarchy of a distributed memory network and integrates signals encoded in other downstream cortical areas that support diverse aspects of knowledge about an object.

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Fig. 1: Location of the perirhinal cortex and its connectivity.
Fig. 2: What emerges in the perirhinal cortex along the ventral visual pathway.
Fig. 3: Linking cue stimuli and target stimuli in the perirhinal cortex.
Fig. 4: Backward output from the perirhinal cortex to lower-order cortical areas for memory retrieval.

References

  1. 1.

    Squire, L. R., Stark, C. E. L. & Clark, R. E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).

    CAS  PubMed  Google Scholar 

  2. 2.

    Andersen, P., Morris, R., Amaral, D., O’Keefe, J. & Bliss, T. Hippocampus Book. (Oxford University Press, 2007).

  3. 3.

    Suzuki, W. A. & Naya, Y. The perirhinal cortex. Annu. Rev. Neurosci. 37, 39–53 (2014).

    CAS  PubMed  Google Scholar 

  4. 4.

    Ranganath, C. & Ritchey, M. Two cortical systems for memory-guided behaviour. Nat. Rev. Neurosci. 13, 713–726 (2012).

    CAS  PubMed  Google Scholar 

  5. 5.

    Miyashita, Y. Cognitive memory: cellular and network machineries and their top-down control. Science 306, 435–440 (2004).

    CAS  PubMed  Google Scholar 

  6. 6.

    Kandel, E. R. et al. Principles of Neural Science. 5th edn, (McGraw-Hill Medical, 2013).

  7. 7.

    Suzuki, W. A. & Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol 350, 497–533 (1994). A monumental article that anatomically characterized the PRC with cortical afferents.

    CAS  PubMed  Google Scholar 

  8. 8.

    Lavenex, P., Suzuki, W. A. & Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J. Comp. Neurol. 447, 394–420 (2002).

    PubMed  Google Scholar 

  9. 9.

    Landi, S. M. & Freiwald, W. A. Two areas for familiar face recognition in the primate brain. Science 357, 591–595 (2017). An fMRI study that revealed that a categorical distinction between familiar and unfamiliar faces occurs initially in the PRC.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Bruce, V. & Young, A. Understanding face recognition. Br. J. Psychol. 77 (Pt 3), 305–327 (1986).

    Google Scholar 

  11. 11.

    Tamura, K. et al. Conversion of object identity to object-general semantic value in the primate temporal cortex. Science 357, 687–692 (2017). An optogenetic study in monkeys demonstrating readout of non-physical representations from PRC neurons for recognition behaviour.

    CAS  PubMed  Google Scholar 

  12. 12.

    Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990). A monumental article that demonstrated a causal linkage between stimulus-selective neuronal firing and its behavioural impact by microstimulation in area MT of monkeys.

    CAS  PubMed  Google Scholar 

  13. 13.

    Salzman, C. D., Murasugi, C. M., Britten, K. H. & Newsome, W. T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).

    CAS  PubMed  Google Scholar 

  14. 14.

    Warrington, E. K. The selective impairment of semantic memory. Q. J. Exp. Psychol. 27, 635–657 (1975).

    CAS  PubMed  Google Scholar 

  15. 15.

    McCarthy, R. A. & Warrington, E. K. Past, present, and prospects: Reflections 40 years on from the selective impairment of semantic memory (Warrington, 1975). Q. J. Exp. Psychol. 69, 1941–1968 (2016).

    Google Scholar 

  16. 16.

    Clarke, A. & Tyler, L. K. Understanding what we see: how we derive meaning from vision. Trends Cogn. Sci. 19, 677–687 (2015).

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Ralph, M. A., Jefferies, E., Patterson, K. & Rogers, T. T. The neural and computational bases of semantic cognition. Nat. Rev. Neurosci. 18, 42–55 (2017). A comprehensive review of human semantic cognition and update of the hub-and-spoke model.

    CAS  PubMed  Google Scholar 

  18. 18.

    Hirabayashi, T., Takeuchi, D., Tamura, K. & Miyashita, Y. Microcircuits for hierarchical elaboration of object coding across primate temporal areas. Science 341, 191–195 (2013). An article that revealed a microcircuit-level mechanism that substantiates the forward progression of associative coding from area TE to the PRC along the ventral visual pathway of monkeys.

    CAS  PubMed  Google Scholar 

  19. 19.

    Hirabayashi, T. & Miyashita, Y. Computational principles of microcircuits for visual object processing in the macaque temporal cortex. Trends Neurosci. 37, 178–187 (2014).

    CAS  PubMed  Google Scholar 

  20. 20.

    Hirabayashi, T., Takeuchi, D., Tamura, K. & Miyashita, Y. Functional microcircuit recruited during retrieval of object association memory in monkey perirhinal cortex. Neuron 77, 192–203 (2013).

    CAS  PubMed  Google Scholar 

  21. 21.

    Koyano, K. W. et al. Laminar module cascade from layer 5 to 6 implementing cue-to-target conversion for object memory retrieval in the primate temporal cortex. Neuron 92, 518–529 (2016).

    CAS  PubMed  Google Scholar 

  22. 22.

    Takeda, M., Koyano, K. W., Hirabayashi, T., Adachi, Y. & Miyashita, Y. Top-down regulation of laminar circuit via inter-area signal for successful object memory recall in monkey temporal cortex. Neuron 86, 840–852 (2015).

    CAS  PubMed  Google Scholar 

  23. 23.

    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  Google Scholar 

  24. 24.

    Wixted, J. T. & Squire, L. R. The medial temporal lobe and the attributes of memory. Trends Cogn. Sci. 15, 210–217 (2011). A comprehensive update on MTL mechanisms of declarative memory.

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    Murray, E. A. & Wise, S. P. Why is there a special issue on perirhinal cortex in a journal called hippocampus? The perirhinal cortex in historical perspective. Hippocampus 22, 1941–1951 (2012).

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Baddeley, A. D. & Warrington, E. K. Amnesia and distinction between long-and short-term memory. J. Verbal Learn. Verbal Behav. 9, 176–189 (1970).

    Google Scholar 

  28. 28.

    Milner, B. Disorders of learning and memory after temporal lobe lesions in man. Clin. Neurosurg. 19, 421–446 (1972).

    CAS  PubMed  Google Scholar 

  29. 29.

    Squire, L. R. & Wixted, J. T. The cognitive neuroscience of human memory since H.M. Annu. Rev. Neurosci. 34, 259–288 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Moscovitch, M., Cabeza, R., Winocur, G. & Nadel, L. Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu. Rev. Psychol. 67, 105–134 (2016).

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Amaral, D. G., Insausti, R. & Cowan, W. M. The entorhinal cortex of the monkey: i. cytoarchitectonic organization. J. Comp. Neurol. 264, 326–355 (1987).

    CAS  PubMed  Google Scholar 

  32. 32.

    Insausti, R., Tunon, T., Sobreviela, T., Insausti, A. M. & Gonzalo, L. M. The human entorhinal cortex: a cytoarchitectonic analysis. J. Comp. Neurol. 355, 171–198 (1995).

    CAS  PubMed  Google Scholar 

  33. 33.

    Insausti, R. et al. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. Am. J. Neuroradiol. 19, 659–671 (1998). A standard reference for the location and borders of the human PRC and adjacent cortical areas determined from MR images using anatomical landmarks defined on the basis of cytoarchitecture.

    CAS  PubMed  Google Scholar 

  34. 34.

    Ding, S. L., Van Hoesen, G. W., Cassell, M. D. & Poremba, A. Parcellation of human temporal polar cortex: a combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers. J. Comp. Neurol. 514, 595–623 (2009).

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Ding, S. L. & Van Hoesen, G. W. Borders, extent, and topography of human perirhinal cortex as revealed using multiple modern neuroanatomical and pathological markers. Hum. Brain Mapp. 31, 1359–1379 (2010). A challenge to the standard definition of the borders of the human PRC. Identified the border between area 36 and area TE more laterally than the conventional border using several cellular, neurochemical, and pathological markers.

    PubMed  Google Scholar 

  36. 36.

    Franko, E., Insausti, A. M., Artacho-Perula, E., Insausti, R. & Chavoix, C. Identification of the human medial temporal lobe regions on magnetic resonance images. Hum. Brain Mapp. 35, 248–256 (2014).

    PubMed  Google Scholar 

  37. 37.

    Burwell, R. D., Witter, M. P. & Amaral, D. G. Perirhinal and postrhinal cortices of the rat: a review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5, 390–408 (1995).

    CAS  PubMed  Google Scholar 

  38. 38.

    Burwell, R. D. & Amaral, D. G. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J. Comp. Neurol. 391, 293–321 (1998).

    CAS  PubMed  Google Scholar 

  39. 39.

    Taylor, K. I. & Probst, A. Anatomic localization of the transentorhinal region of the perirhinal cortex. Neurobiol. Aging 29, 1591–1596 (2008).

    PubMed  Google Scholar 

  40. 40.

    Fujimichi, R. et al. Unitized representation of paired objects in area 35 of the macaque perirhinal cortex. Eur. J. Neurosci. 32, 659–667 (2010).

    PubMed  Google Scholar 

  41. 41.

    Van Essen, D. C., Anderson, C. H. & Felleman, D. J. Information processing in the primate visual system: an integrated systems perspective. Science (New York, N.Y.) 255, 419–423 (1992).

    Google Scholar 

  42. 42.

    Suzuki, W. A. & Amaral, D. G. Where are the periphinal and parahippocampal cortices? A historical overview of the nomenclature and boundaries applied to the primate medial temporal lobe. Neuroscience 120, 893–906 (2003).

    CAS  PubMed  Google Scholar 

  43. 43.

    Saleem, K. S., Price, J. L. & Hashikawa, T. Cytoarchitectonic and chemoarchitectonic subdivisions of the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 500, 973–1006 (2007).

    CAS  PubMed  Google Scholar 

  44. 44.

    Zola-Morgan, S., Squire, L. R., Amaral, D. G. & Suzuki, W. A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J. Neurosci. 9, 4355–4370 (1989).

    CAS  PubMed  Google Scholar 

  45. 45.

    Suzuki, W. A., Zola-Morgan, S., Squire, L. R. & Amaral, D. G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 13, 2430–2451 (1993).

    CAS  PubMed  Google Scholar 

  46. 46.

    Buffalo, E. A. et al. Dissociation between the effects of damage to perirhinal cortex and area TE. Learn. Mem. 6, 572–599 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    CAS  PubMed  Google Scholar 

  48. 48.

    Markov, N. T. et al. Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J. Comp. Neurol. 522, 225–259 (2014).

    PubMed  Google Scholar 

  49. 49.

    Reddy, L. & Kanwisher, N. Coding of visual objects in the ventral stream. Curr. Opin. Neurobiol. 16, 408–414 (2006).

    CAS  PubMed  Google Scholar 

  50. 50.

    Maunsell, J. H. The brain’s visual world: representation of visual targets in cerebral cortex. Science 270, 764–769 (1995).

    CAS  PubMed  Google Scholar 

  51. 51.

    Logothetis, N. K. & Sheinberg, D. L. Visual object recognition. Annu. Rev. Neurosci. 19, 577–621 (1996).

    CAS  PubMed  Google Scholar 

  52. 52.

    Baxter, M. G. Involvement of medial temporal lobe structures in memory and perception. Neuron 61, 667–677 (2009).

    CAS  PubMed  Google Scholar 

  53. 53.

    Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).

    CAS  PubMed  Google Scholar 

  54. 54.

    Tsao, D. Y., Freiwald, W. A., Knutsen, T. A., Mandeville, J. B. & Tootell, R. B. Faces and objects in macaque cerebral cortex. Nat. Neurosci. 6, 989–995 (2003).

    CAS  PubMed  Google Scholar 

  55. 55.

    Nasr, S. & Tootell, R. B. Role of fusiform and anterior temporal cortical areas in facial recognition. NeuroImage 63, 1743–1753 (2012).

    PubMed  PubMed Central  Google Scholar 

  56. 56.

    Tsao, D. Y. & Livingstone, M. S. Mechanisms of face perception. Annu. Rev. Neurosci. 31, 411–437 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Freiwald, W., Duchaine, B. & Yovel, G. Face processing systems: from neurons to real-world social perception. Annu. Rev. Neurosci. 39, 325–346 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Litman, L., Awipi, T. & Davachi, L. Category-specificity in the human medial temporal lobe cortex. Hippocampus 19, 308–319 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59.

    LaRocque, K. F. et al. Global similarity and pattern separation in the human medial temporal lobe predict subsequent memory. J. Neurosci. 33, 5466–5474 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Martin, C. B., McLean, D. A., O’Neil, E. B. & Kohler, S. Distinct familiarity-based response patterns for faces and buildings in perirhinal and parahippocampal cortex. J. Neurosci. 33, 10915–10923 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Collins, J. A. & Dickerson, B. C. Functional connectivity in category-selective brain networks after encoding predicts subsequent memory. Hippocampus, 29, 440–450 (2019).

  62. 62.

    Yamashita, K. et al. Formation of long-term memory representation in human temporal cortex related to pictorial paired associates. J. Neurosci. 29, 10335–10340 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Binney, R. J., Embleton, K. V., Jefferies, E., Parker, G. J. & 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  Google Scholar 

  64. 64.

    Visser, M., Embleton, K. V., Jefferies, E., Parker, G. J. & Ralph, M. A. The inferior, anterior temporal lobes and semantic memory clarified: novel evidence from distortion-corrected fMRI. Neuropsychologia 48, 1689–1696 (2010).

    CAS  PubMed  Google Scholar 

  65. 65.

    Chiou, R. & Lambon Ralph, M. A. The anterior temporal cortex is a primary semantic source of top-down influences on object recognition. Cortex 79, 75–86 (2016).

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Rice, G. E., Hoffman, P., Binney, R. J. & Lambon Ralph, M. A. Concrete versus abstract forms of social concept: an fMRI comparison of knowledge about people versus social terms. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 373, 20170136 (2018).

    Google Scholar 

  67. 67.

    Nobre, A. C., Allison, T. & McCarthy, G. Word recognition in the human inferior temporal lobe. Nature 372, 260 (1994).

    CAS  PubMed  Google Scholar 

  68. 68.

    Noppeney, U. & Price, C. J. A. PET study of stimulus- and task-induced semantic processing. NeuroImage 15, 927–935 (2002).

    CAS  PubMed  Google Scholar 

  69. 69.

    Crinion, J. T., Lambon‐Ralph, M. A., Warburton, E. A., Howard, D. & Wise, R. J. Temporal lobe regions engaged during normal speech comprehension. Brain 126, 1193–1201 (2003).

    PubMed  Google Scholar 

  70. 70.

    Spitsyna, G., Warren, J. E., Scott, S. K., Turkheimer, F. E. & Wise, R. J. Converging language streams in the human temporal lobe. J. Neurosci. 26, 7328–7336 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Xiang, J. Z. & Brown, M. W. Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37, 657–676 (1998). A standard reference for the characteristics and locations of neurons that show repetition suppression in the monkey temporal cortex.

    CAS  PubMed  Google Scholar 

  72. 72.

    Naya, Y., Yoshida, M. & Miyashita, Y. Forward processing of long-term associative memory in monkey inferotemporal cortex. J. Neurosci. 23, 2861–2871 (2003). An article that established that the associative coding first emerges in the PRC by direct comparison between response selectivities of PRC cells and TE cells.

    CAS  PubMed  Google Scholar 

  73. 73.

    Liu, Z. & Richmond, B. J. Response differences in monkey TE and perirhinal cortex: Stimulus association related to reward schedules. J. Neurophysiol. 83, 1677–1692 (2000).

    CAS  PubMed  Google Scholar 

  74. 74.

    Mogami, T. & Tanaka, K. Reward association affects neuronal responses to visual stimuli in macaque TE and perirhinal cortices. J. Neurosci. 26, 6761–6770 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35, 96–111 (1972).

    CAS  PubMed  Google Scholar 

  76. 76.

    Perrett, D. I., Rolls, E. T. & Caan, W. Visual neurones responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982).

    CAS  PubMed  Google Scholar 

  77. 77.

    Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).

    CAS  PubMed  Google Scholar 

  78. 78.

    Gross, C. G. Processing the facial image: a brief history. Am. Psychologist 60, 755–763 (2005).

    Google Scholar 

  79. 79.

    Miyashita, Y. & Chang, H. S. Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 68–70 (1988).

    CAS  PubMed  Google Scholar 

  80. 80.

    Miyashita, Y. Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335, 817–820 (1988). An article that first reported the discovery of the neurons that encode associative long-term memory of objects in the monkey temporal cortex.

    CAS  PubMed  Google Scholar 

  81. 81.

    Sakai, K. & Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991).

    CAS  PubMed  Google Scholar 

  82. 82.

    Miyashita, Y. Inferior temporal cortex: where visual perception meets memory. Annu. Rev. Neurosci. 16, 245–263 (1993).

    CAS  PubMed  Google Scholar 

  83. 83.

    Kobatake, E., Wang, G. & Tanaka, K. Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. J. Neurophysiol. 80, 324–330 (1998).

    CAS  PubMed  Google Scholar 

  84. 84.

    Baker, C. I., Behrmann, M. & Olson, C. R. Impact of learning on representation of parts and wholes in monkey inferotemporal cortex. Nat. Neurosci. 5, 1210–1216 (2002).

    CAS  PubMed  Google Scholar 

  85. 85.

    Freedman, D. J., Riesenhuber, M., Poggio, T. & Miller, E. K. Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. Cereb. Cortex 16, 1631–1644 (2006).

    PubMed  Google Scholar 

  86. 86.

    Meyer, T., Walker, C., Cho, R. Y. & Olson, C. R. Image familiarization sharpens response dynamics of neurons in inferotemporal cortex. Nat. Neurosci. 17, 1388–1394 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Miller, E. K., Li, L. & Desimone, R. A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254, 1377–1379 (1991).

    CAS  PubMed  Google Scholar 

  88. 88.

    Afraz, S. R., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006).

    CAS  PubMed  Google Scholar 

  89. 89.

    Schalk, G. et al. Facephenes and rainbows: causal evidence for functional and anatomical specificity of face and color processing in the human brain. Proc. Natl Acad. Sci. USA 114, 12285–12290 (2017).

    CAS  PubMed  Google Scholar 

  90. 90.

    Moeller, S., Crapse, T., Chang, L. & Tsao, D. Y. The effect of face patch microstimulation on perception of faces and objects. Nat. Neurosci. 20, 743–752 (2017).

    CAS  PubMed  Google Scholar 

  91. 91.

    Afraz, A., Boyden, E. S. & DiCarlo, J. J. Optogenetic and pharmacological suppression of spatial clusters of face neurons reveal their causal role in face gender discrimination. Proc. Natl Acad. Sci. USA 112, 6730–6735 (2015).

    CAS  PubMed  Google Scholar 

  92. 92.

    Sadagopan, S., Zarco, W. & Freiwald, W. A. A causal relationship between face-patch activity and face-detection behavior. Elife 6, e18558 (2017).

    PubMed  PubMed Central  Google Scholar 

  93. 93.

    Gawne, T. J., Kjaer, T. W., Hertz, J. A. & Richmond, B. J. Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cereb. Cortex 6, 482–489 (1996).

    CAS  PubMed  Google Scholar 

  94. 94.

    Yoshida, M., Naya, Y. & Miyashita, Y. Anatomical organization of forward fiber projections from area TE to perirhinal neurons representing visual long-term memory in monkeys. Proc. Natl Acad. Sci. USA 100, 4257–4262 (2003).

    CAS  PubMed  Google Scholar 

  95. 95.

    Hanks, T. D., Ditterich, J. & Shadlen, M. N. Microstimulation of macaque area LIP affects decision-making in a motion discrimination task. Nat. Neurosci. 9, 682–689 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Gold, J. I. & Shadlen, M. N. The neural basis of decision making. Annu. Rev. Neurosci. 30, 535–574 (2007).

    CAS  PubMed  Google Scholar 

  97. 97.

    Kiani, R. & Shadlen, M. N. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 324, 759–764 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 98.

    Hubel, D. H. & Wiesel, T. N. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. London. Ser. B, Biol. Sci. 198, 1–59 (1977).

    CAS  Google Scholar 

  99. 99.

    Alonso, J. M. & Martinez, L. M. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1, 395–403 (1998).

    CAS  PubMed  Google Scholar 

  100. 100.

    Martinez, L. M. et al. Receptive field structure varies with layer in the primary visual cortex. Nat. Neurosci. 8, 372–379 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 101.

    Sakata, S. & Harris, K. D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64, 404–418 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. 102.

    Self, M. W., van Kerkoerle, T., Super, H. & Roelfsema, P. R. Distinct roles of the cortical layers of area v1 in figure-ground segregation. Curr. Biol. 23, 2121–2129 (2013).

    CAS  PubMed  Google Scholar 

  103. 103.

    Douglas, R. J. & Martin, K. A. C. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451 (2004).

    CAS  PubMed  Google Scholar 

  104. 104.

    Harris, K. D. & Shepherd, G. M. The neocortical circuit: themes and variations. Nat. Neurosci. 18, 170–181 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Matsui, T. et al. MRI-based localization of electrophysiological recording sites within the cerebral cortex at single-voxel accuracy. Nat. Methods 4, 161–168 (2007).

    CAS  PubMed  Google Scholar 

  106. 106.

    Takeuchi, D., Hirabayashi, T., Tamura, K. & Miyashita, Y. Reversal of interlaminar signal between sensory and memory processing in monkey temporal cortex. Science. 331, 1443–1447 (2011). An article that demonstrated a context-dependent reversal of interlaminar signal flow in the monkey PRC using current-source-density analysis for identification of cortical layers of the recorded neurons.

    CAS  PubMed  Google Scholar 

  107. 107.

    Kopell, N., Ermentrout, G. B., Whittington, M. A. & Traub, R. D. Gamma rhythms and beta rhythms have different synchronization properties. Proc. Natl Acad. Sci. USA 97, 1867–1872 (2000).

    CAS  PubMed  Google Scholar 

  108. 108.

    Buzsaki, G., Anastassiou, C. A. & Koch, C. The origin of extracellular fields and currents - EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 13, 407–420 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. 109.

    Liebe, S., Hoerzer, G. M., Logothetis, N. K. & Rainer, G. Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nat. Neurosci. 15, 456–U150 (2012).

    CAS  PubMed  Google Scholar 

  110. 110.

    Constantinople, C. M. & Bruno, R. M. Deep cortical layers are activated directly by thalamus. Science 340, 1591–1594 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Insausti, R. & Amaral, D. G. Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents. J. Comp. Neurol. 509, 608–641 (2008).

    PubMed  PubMed Central  Google Scholar 

  112. 112.

    Squire, L. R. & Zola-Morgan, S. The medial temporal lobe memory system. Science 253, 1380–1386 (1991).

    CAS  PubMed  Google Scholar 

  113. 113.

    Brown, M. W. & Aggleton, J. P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2, 51–61 (2001).

    CAS  PubMed  Google Scholar 

  114. 114.

    Eichenbaum, H., Yonelinas, A. P. & Ranganath, C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123–152 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. 115.

    Squire, L. R., Wixted, J. T. & Clark, R. E. Recognition memory and the medial temporal lobe: A new perspective. Nat. Rev. Neurosci. 8, 872–883 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Bowles, B. et al. Impaired familiarity with preserved recollection after anterior temporal-lobe resection that spares the hippocampus. Proc. Natl Acad. Sci. USA 104, 16382–16387 (2007).

    CAS  PubMed  Google Scholar 

  117. 117.

    Wixted, J. T. & Squire, L. R. The role of the human hippocampus in familiarity-based and recollection-based recognition memory. Behav. Brain Res. 215, 197–208 (2010).

    PubMed  PubMed Central  Google Scholar 

  118. 118.

    Meunier, M., Bachevalier, J. & Mishkin, M. Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychologia 35, 999–1015 (1997).

    CAS  PubMed  Google Scholar 

  119. 119.

    Buckley, M. J. & Gaffan, D. Perirhinal cortex ablation impairs visual object identification. J. Neurosci. 18, 2268–2275 (1998).

    CAS  PubMed  Google Scholar 

  120. 120.

    Frey, S. & Petrides, M. Orbitofrontal cortex and memory formation. Neuron 36, 171–176 (2002).

    CAS  PubMed  Google Scholar 

  121. 121.

    Clark, A. M., Bouret, S., Young, A. M., Murray, E. A. & Richmond, B. J. Interaction between orbital prefrontal and rhinal cortex is required for normal estimates of expected value. J. Neurosci. 33, 1833–1845 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. 122.

    Murray, E. A. & Rudebeck, P. H. Specializations for reward-guided decision-making in the primate ventral prefrontal cortex. Nat. Rev. Neurosci. 19, 404–417 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Eichenbaum, H. Prefrontal-hippocampal interactions in episodic memory. Nat. Rev. Neurosci. 18, 547–558 (2017).

    CAS  PubMed  Google Scholar 

  124. 124.

    Tulving, E. & Markowitsch, H. J. Episodic and declarative memory: role of the hippocampus. Hippocampus 8, 198–204 (1998).

    CAS  PubMed  Google Scholar 

  125. 125.

    Eichenbaum, H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41–50 (2000).

    CAS  PubMed  Google Scholar 

  126. 126.

    Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A. & Rosenbaum, R. S. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr. Opin. Neurobiol. 16, 179–190 (2006).

    CAS  PubMed  Google Scholar 

  127. 127.

    Diana, R. A., Yonelinas, A. P. & Ranganath, C. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn. Sci. 11, 379–386 (2007).

    PubMed  Google Scholar 

  128. 128.

    Barsalou, L. W., Kyle Simmons, W., Barbey, A. K. & Wilson, C. D. Grounding conceptual knowledge in modality-specific systems. Trends Cogn. Sci. 7, 84–91 (2003).

    PubMed  Google Scholar 

  129. 129.

    Rogers, T. T. & McClelland, J. L. Semantic Cognition: A Parallel Distributed Processing Approach. (MIT Press, 2004).

  130. 130.

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

    PubMed  Google Scholar 

  131. 131.

    Martin, A. GRAPES—grounding representations in action, perception, and emotion systems: How object properties and categories are represented in the human brain. Psychon. Bull. Rev. 23, 979–990 (2016). A comprehensive review of the human semantic memory system and an update of its distributed representation model.

    PubMed  PubMed Central  Google Scholar 

  132. 132.

    Hodges, J. R., Patterson, K., Oxbury, S. & Funnell, E. Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. Brain 115, 1783–1806 (1992).

    PubMed  Google Scholar 

  133. 133.

    Hodges, J. R. & Patterson, K. Semantic dementia: a unique clinicopathological syndrome. Lancet Neurol. 6, 1004–1014 (2007).

    CAS  PubMed  Google Scholar 

  134. 134.

    Sharon, T., Moscovitch, M. & Gilboa, A. Rapid neocortical acquisition of long-term arbitrary associations independent of the hippocampus. Proc. Natl Acad. Sci. USA 108, 1146–1151 (2011). An article that reported the ‘fast mapping’ procedure, claiming that long-term arbitrary associations can be acquired independently of the hippocampus.

    CAS  PubMed  Google Scholar 

  135. 135.

    Smith, C. N., Urgolites, Z. J., Hopkins, R. O. & Squire, L. R. Comparison of explicit and incidental learning strategies in memory-impaired patients. Proc. Natl Acad. Sci. USA 111, 475–479 (2014).

    CAS  PubMed  Google Scholar 

  136. 136.

    Greve, A., Cooper, E. & Henson, R. N. No evidence that ‘fast-mapping’ benefits novel learning in healthy older adults. Neuropsychologia 60, 52–59 (2014).

    PubMed  PubMed Central  Google Scholar 

  137. 137.

    Merhav, M., Karni, A. & Gilboa, A. Neocortical catastrophic interference in healthy and amnesic adults: a paradoxical matter of time. Hippocampus 24, 1653–1662 (2014).

    PubMed  Google Scholar 

  138. 138.

    Merhav, M., Karni, A. & Gilboa, A. Not all declarative memories are created equal: Fast Mapping as a direct route to cortical declarative representations. NeuroImage 117, 80–92 (2015).

    PubMed  Google Scholar 

  139. 139.

    Coutanche, M. N. & Thompson-Schill, S. L. Rapid consolidation of new knowledge in adulthood via fast mapping. Trends Cogn. Sci. 19, 486–488 (2015).

    PubMed  PubMed Central  Google Scholar 

  140. 140.

    Cooper, E., Greve, A. & Henson, R. N. Little evidence for fast mapping (FM) in adults: a review and discussion. Cogn. Neurosci. https://doi.org/10.1080/17588928.2018.1542376 (2018).

    PubMed  Google Scholar 

  141. 141.

    Moran, M. A., Mufson, E. J. & Mesulam, M. M. Neural inputs into the temporopolar cortex of the rhesus monkey. J. Comp. Neurol. 256, 88–103 (1987).

    CAS  PubMed  Google Scholar 

  142. 142.

    Pascual, B. et al. Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study. Cereb. Cortex 25, 680–702 (2015).

    PubMed  Google Scholar 

  143. 143.

    Higuchi, S. & Miyashita, Y. Formation of mnemonic neuronal responses to visual paired associates in inferotemporal cortex is impaired by perirhinal and entorhinal lesions. Proc. Natl Acad. Sci. USA 93, 739–743 (1996).

    CAS  PubMed  Google Scholar 

  144. 144.

    Naya, Y., Yoshida, M. & Miyashita, Y. Backward spreading of memory-retrieval signal in the primate temporal cortex. Science 291, 661–664 (2001).

    CAS  PubMed  Google Scholar 

  145. 145.

    Chan, A. M. et al. First-pass selectivity for semantic categories in human anteroventral temporal lobe. J. Neurosci. 31, 18119–18129 (2011). An article that revealed the activation dynamics of lexicosemantic representations in the human anterior ventral cortex, suggesting a ‘first-pass’ activation of the PRC, followed by the backward activation of posterior temporal areas for iconic/visual form representations.

    CAS  PubMed  PubMed Central  Google Scholar 

  146. 146.

    Chen, R., Wang, F., Liang, H. & Li, W. Synergistic processing of visual contours across cortical layers in V1 and V2. Neuron 96, 1388–1402 e1384 (2017).

    CAS  PubMed  Google Scholar 

  147. 147.

    Pobric, G., Jefferies, E. & 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  Google Scholar 

  148. 148.

    Squire, L. R., Knowlton, B. & Musen, G. The structure and organization of memory. Annu. Rev. Psychol. 44, 453–495 (1993).

    CAS  PubMed  Google Scholar 

  149. 149.

    Kanwisher, N. Functional specificity in the human brain: a window into the functional architecture of the mind. Proc. Natl Acad. Sci. USA 107, 11163–11170 (2010).

    CAS  PubMed  Google Scholar 

  150. 150.

    Dudai, Y. The restless engram: consolidations never end. Annu. Rev. Neurosci. 35, 227–247 (2012).

    CAS  PubMed  Google Scholar 

  151. 151.

    Wang, S.-H. & Morris, R. G. M. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 61, 49–79 (2010).

    PubMed  Google Scholar 

  152. 152.

    Balderas, I., Rodriguez-Ortiz, C. J. & Bermudez-Rattoni, F. Consolidation and reconsolidation of object recognition memory. Behav. Brain Res. 285, 213–222 (2015).

    PubMed  Google Scholar 

  153. 153.

    Miranda, M. & Bekinschtein, P. Plasticity mechanisms of memory consolidation and reconsolidation in the perirhinal cortex. Neurosci. 370, 46–61 (2018).

    CAS  Google Scholar 

  154. 154.

    Eacott, M. J., Gaffan, D. & Murray, E. A. Preserved recognition memory for small sets, and impaired stimulus identification for large sets, following rhinal cortex ablations in monkeys. Eur. J. Neurosci. 6, 1466–1478 (1994). An article that first proposed the involvement of the rhinal cortex (that is, the ERC plus the PRC) in visual identification and perceptual function, a hypothesis later known as the perceptual–mnemonic hypothesis of the PRC function.

    CAS  PubMed  Google Scholar 

  155. 155.

    Buckley, M. J. & Gaffan, D. Impairment of visual object-discrimination learning after perirhinal cortex ablation. Behav. Neurosci. 111, 467–475 (1997).

    CAS  PubMed  Google Scholar 

  156. 156.

    Buckley, M. J., Booth, M. C. A., Rolls, E. T. & Gaffan, D. Selective perceptual impairments after perirhinal cortex ablation. J. Neurosci. 21, 9824–9836 (2001).

    CAS  PubMed  Google Scholar 

  157. 157.

    Bussey, T. J. & Saksida, L. M. The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur. J. Neurosci. 15, 355–364 (2002).

    PubMed  Google Scholar 

  158. 158.

    Bussey, T. J., Saksida, L. M. & Murray, E. A. Perirhinal cortex resolves feature ambiguity in complex visual discriminations. Eur. J. Neurosci. 15, 365–374 (2002).

    PubMed  Google Scholar 

  159. 159.

    Bussey, T. J., Saksida, L. M. & Murray, E. A. Impairments in visual discrimination after perirhinal cortex lesions: testing ‘declarative’ vs. ‘perceptual-mnemonic’ views of perirhinal cortex function. Eur. J. Neurosci. 17, 649–660 (2003).

    PubMed  Google Scholar 

  160. 160.

    Bartko, S. J., Winters, B. D., Cowell, R. A., Saksida, L. M. & Bussey, T. J. Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks. Learn. Mem. 14, 821–832 (2007).

    Google Scholar 

  161. 161.

    Bartko, S. J., Winters, B. D., Cowell, R. A., Saksida, L. M. & Bussey, T. J. Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J. Neurosci. 27, 2548–2559 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  162. 162.

    Lee, A. C. et al. Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view. Neuropsychologia 43, 1–11 (2005).

    PubMed  Google Scholar 

  163. 163.

    Lee, A. C. et al. Differentiating the roles of the hippocampus and perirhinal cortex in processes beyond long-term declarative memory: a double dissociation in dementia. J. Neurosci. 26, 5198–5203 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. 164.

    Erez, J., Lee, A. C. & Barense, M. D. It does not look odd to me: perceptual impairments and eye movements in amnesic patients with medial temporal lobe damage. Neuropsychologia 51, 168–180 (2013).

    PubMed  PubMed Central  Google Scholar 

  165. 165.

    Behrmann, M., Lee, A. C., Geskin, J. Z., Graham, K. S. & Barense, M. D. Temporal lobe contribution to perceptual function: A tale of three patient groups. Neuropsychologia 90, 33–45 (2016).

    CAS  PubMed  Google Scholar 

  166. 166.

    Buffalo, E. A., Ramus, S. J., Squire, L. R. & Zola, S. M. Perception and recognition memory in monkeys following lesions of area TE and perirhinal cortex. Learn. Mem. 7, 375–382 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. 167.

    Hampton, R. R. Monkey perirhinal cortex is critical for visual memory, but not for visual perception: reexamination of the behavioural evidence from monkeys. Q. J. Exp. Psychol. Sect. B Comp. Physiol. Psychol. 58, 283–299 (2005).

    Google Scholar 

  168. 168.

    Clark, R. E., Reinagel, P., Broadbent, N. J., Flister, E. D. & Squire, L. R. Intact performance on feature-ambiguous discriminations in rats with lesions of the perirhinal cortex. Neuron 70, 132–140 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  169. 169.

    Levy, D. A., Shrager, Y. & Squire, L. R. Intact visual discrimination of complex and feature-ambiguous stimuli in the absence of perirhinal cortex. Learn. Mem. 12, 61–66 (2005).

    Google Scholar 

  170. 170.

    Shrager, Y., Gold, J. J., Hopkins, R. O. & Squire, L. R. Intact visual perception in memory-impaired patients with medial temporal lobe lesions. J. Neurosci. 26, 2235–2240 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. 171.

    Knutson, A. R., Hopkins, R. O. & Squire, L. R. Visual discrimination performance, memory, and medial temporal lobe function. Proc. Natl Acad. Sci. USA 109, 13106–13111 (2012).

    CAS  PubMed  Google Scholar 

  172. 172.

    Urgolites, Z. J., Hopkins, R. O. & Squire, L. R. Medial temporal lobe and topographical memory. Proc. Natl Acad. Sci. USA 114, 8626–8630 (2017).

    CAS  PubMed  Google Scholar 

  173. 173.

    Miyamoto, K. et al. Causal neural network of metamemory for retrospection in primates. Science 355, 188–193 (2017). An article that reported the discovery of metacognitive centres for retrospection in the anterior dorsal PFC in monkeys.

    CAS  PubMed  Google Scholar 

  174. 174.

    Miyamoto, K., Setsuie, R., Osada, T. & Miyashita, Y. Reversible silencing of the frontopolar cortex selectively impairs metacognitive judgment on non-experience in primates. Neuron 97, 980–989 (2018).

    CAS  PubMed  Google Scholar 

  175. 175.

    Li, L., Miller, E. K. & Desimone, R. The representation of stimulus familiarity in anterior inferior temporal cortex. J. Neurophysiol. 69, 1918–1929 (1993).

    CAS  PubMed  Google Scholar 

  176. 176.

    Woloszyn, L. & Sheinberg, D. L. Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex. Neuron 74, 193–205 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  177. 177.

    Sakai, K. & Miyashita, Y. Neuronal tuning to learned complex forms in vision. Neuroreport 5, 829–832 (1994).

    CAS  PubMed  Google Scholar 

  178. 178.

    Brown, M. W., Wilson, F. A. & Riches, I. P. Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory. Brain Res. 409, 158–162 (1987).

    CAS  PubMed  Google Scholar 

  179. 179.

    Miller, E. K., Li, L. & Desimone, R. Activity of neurons in anterior inferior temporal cortex during a short-term memory task. J. Neurosci. 13, 1460–1478 (1993).

    CAS  PubMed  Google Scholar 

  180. 180.

    Sobotka, S. & Ringo, J. L. Investigation of long-term recognition and association memory in unit responses from inferotemporal cortex. Exp. Brain Res. 96, 28–38 (1993).

    CAS  PubMed  Google Scholar 

  181. 181.

    McMahon, D. B. & Olson, C. R. Repetition suppression in monkey inferotemporal cortex: relation to behavioral priming. J. Neurophysiol. 97, 3532–3543 (2007).

    PubMed  Google Scholar 

  182. 182.

    Schroeder, C. E., Mehta, A. D. & Givre, S. J. A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. Cereb. Cortex 8, 575–592 (1998).

    CAS  PubMed  Google Scholar 

  183. 183.

    Cash, S. S. et al. The human K-complex represents an isolated cortical down-state. Science 324, 1084–1087 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  184. 184.

    Nicholson, C. & Freeman, J. A. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J. Neurophysiol. 38, 356–368 (1975).

    CAS  PubMed  Google Scholar 

  185. 185.

    Freeman, J. A. & Nicholson, C. Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 38, 369–382 (1975).

    CAS  PubMed  Google Scholar 

  186. 186.

    Mitzdorf, U. Current source-density method and application in cat cerebral cortex: investigation of evoked-potentials and EEG phenomena. Physiol. Rev. 65, 37–100 (1985).

    CAS  PubMed  Google Scholar 

  187. 187.

    Squire, L. R. Memory and Brain. Oxford University Press, Oxford (1987).

    Google Scholar 

  188. 188.

    Clayton, N. S. & Dickinson, A. Episodic-like memory during cache recovery by scrub jays. Nature 395, 272–274 (1998).

    CAS  PubMed  Google Scholar 

  189. 189.

    Clayton, N. S., Bussey, T. J. & Dickinson, A. Can animals recall the past and plan for the future? Nat. Rev. Neurosci. 4, 685–691 (2003).

    CAS  PubMed  Google Scholar 

  190. 190.

    Lambon Ralph, M. A., Sage, K., Jones, R. W. & Mayberry, E. J. Coherent concepts are computed in the anterior temporal lobes. Proc. Natl Acad. Sci. USA 107, 2717–2722 (2010).

    CAS  PubMed  Google Scholar 

  191. 191.

    Colombo, M. & Gross, C. G. Responses of inferior temporal cortex and hippocampal-neurons during delayed matching-to-sample in monkeys (Macaca fascicularis). Behav. Neurosci. 108, 443–455 (1994).

    CAS  PubMed  Google Scholar 

  192. 192.

    Gibson, J. R. & Maunsell, J. H. Sensory modality specificity of neural activity related to memory in visual cortex. J. Neurophysiol. 78, 1263–1275 (1997).

    CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported in part by MEXT and the Japan Society for the Promotion of Science KAKENHI grants 17H06161 and 24220008.

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Glossary

Structural encoding

An early-stage encoding process in cognition that emphasizes the physical structure of the stimulus. Automatically proceeds even in a shallow encoding condition. Particularly well analysed and theorized in face recognition.

Ventral visual pathway

A functional stream involved in visual analyses of objects in the primate brain. Also called the ‘what pathway’. Anatomically, visual input from area V1 is projected to areas TEO and TE via areas V2 and V4.

Nested associations

In a semantic network model, nodes and arcs are hierarchically organized to form associative knowledge representations. Spreading activation along the arcs retrieves the nested associative representation.

Hub-and-spoke model

A hypothesis of the structure and neural basis of semantic memory. Many cortical regions represent an aspect of conceptual knowledge that is modality specific. The links between each modality-specific region and a supramodal hub region are called ‘spokes’.

Recency neurons

A group of neurons in the anterior temporal cortex of monkeys that encode information whether or not a stimulus has been seen recently, regardless of whether it is relatively familiar or not.

Repetition priming

Improvements in a behavioural response when stimuli are repeatedly presented. The improvements can be measured in terms of accuracy or reaction time.

Agranular cortex

A cytoarchitecturally defined term denoting the type of heterotypic cortex that is distinguished by the lack of granule cells. An area of cortex that is only slightly granulated is termed ‘dysgranular’.

Lexicosemantic association area

Brain areas that are devoted to the analysis and understanding of the meaning of the lexical units (words and subwords) and of the relations between the word meaning and structure of the language.

Current sink

From extracellular electric potentials recorded at multiple sites, current sources and sinks generating the measured potentials are estimated. Typically, the current sinks indicate the locations of synapses generating excitatory postsynaptic potentials.

Receptive fields

Portions of sensory space that can elicit neuronal responses when stimulated. In vision, the sensory space can be defined in multiple dimensions, such as space, time and tuning properties.

Matching-to-sample test

A form of conditional discrimination. Short-term memory or working memory has been studied with this test. A participant is asked to first encode a stimulus and later to make a forced-choice response among options where one option corresponds to that stimulus.

Cross-modal matching test

In the matching-to-sample test, the correct response option typically corresponds directly in some way to the stimulus (for example, the response option and stimulus are the same colour). However, the test can require a symbolic match or a matching based on the identity of the object. For example, participants are asked to cross-modally match visual and auditory displays on the basis of the identity of the speaker or sound source.

Face-patch network

Specialized brain areas that primates have evolved to extract multidimensional facial information are called ‘face patches’. They are tightly and specifically interconnected to form a face-processing system.

Repetition suppression

The reduction in neural activity when stimuli are repeated. It can occur across a range of repetition time lags, even when multiple interleaving stimuli are presented with the repeated stimulus.

Stimulus–reward associations

An ability to assign value to stimuli, or to link objects with the affective qualities of reward, on the basis of reinforcement history. Amygdala plays a key role in this association.

Trigger features

A particular feature of a stimulant which causes a reaction within a particular neuron. In the primate temporal cortex, trigger features become complex, including hands or faces.

Cued-recall task

A procedure for testing memory in which a participant is presented with cues, such as words or objects, to aid recall of previously experienced stimuli. Cued recall also occurs in everyday life.

Memory traces

A transient or long-term change in the brain that provides a physical basis for the persistence of memory. Also called ‘memory engram’.

Retrospection

A reconsideration of something that happened in the past, typically of something involving one’s own experiences.

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Miyashita, Y. Perirhinal circuits for memory processing. Nat Rev Neurosci 20, 577–592 (2019). https://doi.org/10.1038/s41583-019-0213-6

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