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.

  • Review Article
  • Published:

Integration of objects and space in perception and memory

Abstract

Distinct processing of objects and space has been an organizing principle for studying higher-level vision and medial temporal lobe memory. Here, however, we discuss how object and spatial information are in fact closely integrated in vision and memory. The ventral, object-processing visual pathway carries precise spatial information, transformed from retinotopic coordinates into relative dimensions. At the final stages of the ventral pathway, including the dorsal anterior temporal lobe (TEd), object-sensitive neurons are intermixed with neurons that process large-scale environmental space. TEd projects primarily to perirhinal cortex (PRC), which in turn projects to lateral entorhinal cortex (LEC). PRC and LEC also combine object and spatial information. For example, PRC and LEC neurons exhibit place fields that are evoked by landmark objects or the remembered locations of objects. Thus, spatial information, on both local and global scales, is deeply integrated into the ventral (temporal) object-processing pathway in vision and memory.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Transformation of retinotopic information into contour coding in area V4.
Figure 2: Transformation of retinotopic information into surface coding in TE.
Figure 3: Transformation of retinotopic information into medial axis coding in TE.
Figure 4: Neural coding of face structure in highly composite dimensions.
Figure 5: Large-scale environmental shape information in TE.
Figure 6: LEC responses to objects in freely moving rats.
Figure 7: Object–space responses in LEC and hippocampus.

Similar content being viewed by others

References

  1. Mishkin, M., Ungerleider, L.G. & Macko, K.A. Object vision and spatial vision: two cortical pathways. Trends Neurosci. 6, 414–417 (1983).This seminal paper distinguished the dorsal and ventral visual pathways.

    Article  Google Scholar 

  2. Wilson, F.A., Scalaidhe, S.P. & Goldman-Rakic, P.S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1958 (1993).

    Article  CAS  PubMed  Google Scholar 

  3. Kaas, J.H. & Hackett, T.A. 'What' and 'where' processing in auditory cortex. Nat. Neurosci. 2, 1045–1047 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Romanski, L.M. et al. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 2, 1131–1136 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. McNaughton, B.L., Leonard, B. & Chen, L.L. Cortical-hippocampal interactions and cognitive mapping: a hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing. Psychobiology 17, 230–235 (1989).

    Article  Google Scholar 

  6. Goodale, M.A. & Milner, A.D. Separate visual pathways for perception and action. Trends Neurosci. 15, 20–25 (1992).

    Article  CAS  PubMed  Google Scholar 

  7. Kravitz, D.J., Saleem, K.S., Baker, C.I. & Mishkin, M. A new neural framework for visuospatial processing. Nat. Rev. Neurosci. 12, 217–230 (2011).This comprehensive review reorganizes the dorsal visual pathway in terms of its output functionalities.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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).This reconsideration of ventral pathway organization reveals greater complexity and diversity in connectivity.

    Article  PubMed  Google Scholar 

  9. Witter, M.P. & Amaral, D.G. in The Rat Nervous System 3rd edn. (ed. Paxinos, G.) 635–704 (Elsevier, Amsterdam, 2004).

  10. Burwell, R.D. The parahippocampal region: corticocortical connectivity. Ann. NY Acad. Sci. 911, 25–42 (2000).This article summarizes the data in rodents regarding parallel pathways from the perirhinal cortex and postrhinal cortex to the hippocampus, via the lateral and medial entorhinal cortical regions, respectively.

    Article  CAS  PubMed  Google Scholar 

  11. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).

  12. Suzuki, W.A., Miller, E.K. & Desimone, R. Object and place memory in the macaque entorhinal cortex. J. Neurophysiol. 78, 1062–1081 (1997).

    Article  CAS  PubMed  Google Scholar 

  13. Gaffan, D. Idiothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: a review. Exp. Brain Res. 123, 201–209 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Manns, J.R. & Eichenbaum, H. Evolution of declarative memory. Hippocampus 16, 795–808 (2006).

    Article  PubMed  Google Scholar 

  15. Knierim, J.J., Lee, I. & Hargreaves, E.L. Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16, 755–764 (2006).

    Article  PubMed  Google Scholar 

  16. 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).

    Article  PubMed  Google Scholar 

  17. Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).This is a comprehensive and well-known version of the visual system wiring diagram.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  19. Kobatake, E. & Tanaka, K. Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J. Neurophysiol. 71, 856–867 (1994).

    Article  CAS  PubMed  Google Scholar 

  20. Ullman, S. Aligning pictorial descriptions: an approach to object recognition. Cognition 32, 193–254 (1989).

    Article  CAS  PubMed  Google Scholar 

  21. Vetter, T., Hurlbert, A. & Poggio, T. View-based models of 3D object recognition: invariance to imaging transformations. Cereb. Cortex 5, 261–269 (1995).

    Article  CAS  PubMed  Google Scholar 

  22. Bülthoff, H.H., Edelman, S.Y. & Tarr, M.J. How are three-dimensional objects represented in the brain? Cereb. Cortex 5, 247–260 (1995).

    Article  PubMed  Google Scholar 

  23. Li, N. & DiCarlo, J.J. Unsupervised natural experience rapidly alters invariant object representation in visual cortex. Science 321, 1502–1507 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hubel, D.H. & Wiesel, T.N. Receptive fields of single neurones in the cat's striate cortex. J. Physiol. (Lond.) 148, 574–591 (1959).

    Article  CAS  Google Scholar 

  25. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  26. Pasupathy, A. & Connor, C.E. Responses to contour features in macaque area V4. J. Neurophysiol. 82, 2490–2502 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Pasupathy, A. & Connor, C.E. Shape representation in area V4: position-specific tuning for boundary conformation. J. Neurophysiol. 86, 2505–2519 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. Sharpee, T.O., Kouh, M. & Reynolds, J.H. Trade-off between curvature tuning and position invariance in visual area V4. Proc. Natl. Acad. Sci. USA 110, 11618–11623 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nandy, A.S., Sharpee, T.O., Reynolds, J.H. & Mitchell, J.F. The fine structure of shape tuning in area V4. Neuron 78, 1102–1115 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Yau, J.M., Pasupathy, A., Brincat, S.L. & Connor, C.E. Curvature processing dynamics in macaque area V4. Cereb. Cortex 23, 198–209 (2013).

    Article  PubMed  Google Scholar 

  31. Bushnell, B.N., Harding, P.J., Kosai, Y. & Pasupathy, A. Partial occlusion modulates contour-based shape encoding in primate area V4. J. Neurosci. 31, 4012–4024 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kosai, Y., El-Shamayleh, Y., Fyall, A.M. & Pasupathy, A. The role of visual area V4 in the discrimination of partially occluded shapes. J. Neurosci. 34, 8570–8584 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Oleskiw, T.D., Pasupathy, A. & Bair, W. Spectral receptive fields do not explain tuning for boundary curvature in V4. J. Neurophysiol. 112, 2114–2122 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  34. El-Shamayleh, Y. & Pasupathy, A. Contour curvature as an invariant code for objects in visual area V4. J. Neurosci. 36, 5532–5543 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gallant, J.L., Braun, J. & Van Essen, D.C. Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. Science 259, 100–103 (1993).

    Article  CAS  PubMed  Google Scholar 

  36. Janssen, P., Vogels, R. & Orban, G.A. Macaque inferior temporal neurons are selective for disparity-defined three-dimensional shapes. Proc. Natl. Acad. Sci. USA 96, 8217–8222 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Janssen, P., Vogels, R. & Orban, G.A. Three-dimensional shape coding in inferior temporal cortex. Neuron 27, 385–397 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Yamane, Y., Carlson, E.T., Bowman, K.C., Wang, Z. & Connor, C.E. A neural code for three-dimensional object shape in macaque inferotemporal cortex. Nat. Neurosci. 11, 1352–1360 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hung, C.C., Carlson, E.T. & Connor, C.E. Medial axis shape coding in macaque inferotemporal cortex. Neuron 74, 1099–1113 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Vaziri, S. & Connor, C.E. Representation of gravity-aligned scene structure in ventral pathway visual cortex. Curr. Biol. 26, 766–774 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Verhoef, B.E., Vogels, R. & Janssen, P. Inferotemporal cortex subserves three-dimensional structure categorization. Neuron 73, 171–182 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Nevatia, R. & Binford, T.O. Description and recognition of curved objects. Artificial Intelligence 8, 77–98 (1977).

    Article  Google Scholar 

  43. Blum, H. Biological shape and visual science. I. J. Theor. Biol. 38, 205–287 (1973).

    Article  CAS  PubMed  Google Scholar 

  44. Marr, D. & Nishihara, H.K. Representation and recognition of the spatial organization of three-dimensional shapes. Proc. R. Soc. Lond. B Biol. Sci. 200, 269–294 (1978).

    Article  CAS  PubMed  Google Scholar 

  45. Biederman, I. Recognition-by-components: a theory of human image understanding. Psychol. Rev. 94, 115–147 (1987).

    Article  PubMed  Google Scholar 

  46. Leyton, M. A Generative Theory of Shape (Springer, Berlin 2001).

  47. Kimia, B.B. On the role of medial geometry in human vision. J. Physiol. Paris 97, 155–190 (2003).

    Article  PubMed  Google Scholar 

  48. Feldman, J. & Singh, M. Bayesian estimation of the shape skeleton. Proc. Natl. Acad. Sci. USA 103, 18014–18019 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lee, T.S., Mumford, D., Romero, R. & Lamme, V.A. The role of the primary visual cortex in higher level vision. Vision Res. 38, 2429–2454 (1998).

    Article  CAS  PubMed  Google Scholar 

  50. Vaziri, S., Carlson, E.T., Wang, Z. & Connor, C.E. A channel for 3D environmental shape in anterior inferotemporal cortex. Neuron 84, 55–62 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Connor, C.E., Gallant, J.L., Preddie, D.C. & Van Essen, D.C. Responses in area V4 depend on the spatial relationship between stimulus and attention. J. Neurophysiol. 75, 1306–1308 (1996).

    Article  CAS  PubMed  Google Scholar 

  52. Connor, C.E., Preddie, D.C., Gallant, J.L. & Van Essen, D.C. Spatial attention effects in macaque area V4. J. Neurosci. 17, 3201–3214 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Pasupathy, A. & Connor, C.E. Population coding of shape in area V4. Nat. Neurosci. 5, 1332–1338 (2002).

    Article  CAS  PubMed  Google Scholar 

  54. Brincat, S.L. & Connor, C.E. Underlying principles of visual shape selectivity in posterior inferotemporal cortex. Nat. Neurosci. 7, 880–886 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. Brincat, S.L. & Connor, C.E. Dynamic shape synthesis in posterior inferotemporal cortex. Neuron 49, 17–24 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. Chang, L. & Tsao, D.Y. The code for facial identity in the primate brain. Cell 169, 1013–1028.e14 (2017).This paradigmatic coding analysis makes a conclusive case for ramp-coding along highly composite linear dimensions in facial structure space.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Freiwald, W.A., Tsao, D.Y. & Livingstone, M.S. A face feature space in the macaque temporal lobe. Nat. Neurosci. 12, 1187–1196 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Leopold, D.A., Bondar, I.V. & Giese, M.A. Norm-based face encoding by single neurons in the monkey inferotemporal cortex. Nature 442, 572–575 (2006).

    Article  CAS  PubMed  Google Scholar 

  59. Hong, H., Yamins, D.L., Majaj, N.J. & DiCarlo, J.J. Explicit information for category-orthogonal object properties increases along the ventral stream. Nat. Neurosci. 19, 613–622 (2016).Hong et al . show that more information about position, etc. can be decoded from a population of IT neurons compared to an equal number of V4 neurons. This might reflect the smaller receptive fields of V4 neurons, which necessarily carry information about less visual space, but in any case demonstrates that position information is not lost in IT. This does not mean that it is retinotopic information, which seems unlikely given the scale of IT receptive fields. Instead, it seems likely to be information about position relative to the (comparatively small) viewing aperture, the fixation point or background features.

    Article  CAS  PubMed  Google Scholar 

  60. Konkle, T. & Oliva, A. A real-world size organization of object responses in occipitotemporal cortex. Neuron 74, 1114–1124 (2012).This study shows that object representations in human ventral pathway exhibit a small-to-large dorsal–ventral gradient, based on perceived size rather than retinotopic extent.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Srihasam, K., Vincent, J.L. & Livingstone, M.S. Novel domain formation reveals proto-architecture in inferotemporal cortex. Nat. Neurosci. 17, 1776–1783 (2014).This paper shows that object-value training in young monkeys produces dedicated processing regions in ventral pathway cortex organized by the shape characteristics of the learned objects.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ponce, C.R., Hartmann, T.S. & Livingstone, M.S. End-stopping predicts curvature tuning along the ventral stream. J. Neurosci. 37, 648–659 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 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). This landmark paper initiated the study of category-specific patches in ventral pathway cortex with the discovery of the fusiform face area.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Kornblith, S., Cheng, X., Ohayon, S. & Tsao, D.Y. A network for scene processing in the macaque temporal lobe. Neuron 79, 766–781 (2013).This group used fMRI and microelectrode recording to study place processing in a patch of monkey occipitotemporal visual cortex that could correspond to the human parahippocampal place area.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).This paper was the first to report the existence of the parahippocampal place area in human visual cortex.

    Article  CAS  PubMed  Google Scholar 

  66. Lafer-Sousa, R. & Conway, B.R. Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat. Neurosci. 16, 1870–1878 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Verhoef, B.E., Bohon, K.S. & Conway, B.R. Functional architecture for disparity in macaque inferior temporal cortex and its relationship to the architecture for faces, color, scenes, and visual field. J. Neurosci. 35, 6952–6968 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lafer-Sousa, R., Conway, B.R. & Kanwisher, N.G. Color-biased regions of the ventral visual pathway lie between face- and place-selective regions in humans, as in macaques. J. Neurosci. 36, 1682–1697 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Arcaro, M.J. & Livingstone, M.S. Retinotopic organization of scene areas in macaque inferior temporal cortex. J. Neurosci. 37, 7373–7389 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Scoville, W.B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).The classic case report of the famous patient with amnesia H.M.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Meunier, M., Bachevalier, J., Mishkin, M. & Murray, E.A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci. 13, 5418–5432 (1993). This and the following reference provided strong evidence that damage to the PRC, not the hippocampus proper, was the primary cause of the mnemonic deficits in the DNMS task of visual recognition memory.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Meunier, M., Hadfield, W., Bachevalier, J. & Murray, E.A. Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J. Neurophysiol. 75, 1190–1205 (1996).

    Article  CAS  PubMed  Google Scholar 

  73. Murray, E.A. & Bussey, T.J. Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn. Sci. 3, 142–151 (1999).This article proposes that the perirhinal cortex should be viewed as processing high-order perceptual information as well as memory.

    Article  CAS  PubMed  Google Scholar 

  74. Bussey, T.J., Saksida, L.M. & Murray, E.A. The perceptual-mnemonic/feature conjunction model of perirhinal cortex function. Q. J. Exp. Psychol. B 58, 269–282 (2005).

    Article  PubMed  Google Scholar 

  75. 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).This paper puts forth the provocative argument that the perirhinal cortex should not be considered a component of the medial temporal lobe memory system but rather a part of sensory neocortex.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Suzuki, W.A. Perception and the medial temporal lobe: evaluating the current evidence. Neuron 61, 657–666 (2009).

    Article  CAS  PubMed  Google Scholar 

  77. Norman, G. & Eacott, M.J. Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav. Neurosci. 119, 557–566 (2005).

    Article  CAS  PubMed  Google Scholar 

  78. Jo, Y.S. & Lee, I. Perirhinal cortex is necessary for acquiring, but not for retrieving object-place paired association. Learn. Mem. 17, 97–103 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Jo, Y.S. & Lee, I. Disconnection of the hippocampal-perirhinal cortical circuits severely disrupts object-place paired associative memory. J. Neurosci. 30, 9850–9858 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Wilson, D.I. et al. Lateral entorhinal cortex is critical for novel object-context recognition. Hippocampus 23, 352–366 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Wilson, D.I., Watanabe, S., Milner, H. & Ainge, J.A. Lateral entorhinal cortex is necessary for associative but not nonassociative recognition memory. Hippocampus 23, 1280–1290 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Hunsaker, M.R., Chen, V., Tran, G.T. & Kesner, R.P. The medial and lateral entorhinal cortex both contribute to contextual and item recognition memory: a test of the binding of items and context model. Hippocampus 23, 380–391 (2013).

    Article  PubMed  Google Scholar 

  83. Stouffer, E.M. & Klein, J.E. Lesions of the lateral entorhinal cortex disrupt non-spatial latent learning but spare spatial latent learning in the rat (Rattus norvegicus). Acta Neurobiol. Exp. (Warsz.) 73, 430–437 (2013).

    Google Scholar 

  84. Heimer-McGinn, V.R., Poeta, D.L., Aghi, K., Udawatta, M. & Burwell, R.D. Disconnection of the perirhinal and postrhinal cortices impairs recognition of objects in context but not contextual fear conditioning. J. Neurosci. 37, 4819–4829 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Liu, P. & Bilkey, D.K. The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav. Neurosci. 115, 94–111 (2001).

    Article  CAS  PubMed  Google Scholar 

  86. Bachevalier, J. & Nemanic, S. Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus 18, 64–80 (2008).

    Article  PubMed  Google Scholar 

  87. Van Cauter, T. et al. Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb. Cortex 23, 451–459 (2013).

    Article  PubMed  Google Scholar 

  88. Hunsaker, M.R., Mooy, G.G., Swift, J.S. & Kesner, R.P. Dissociations of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. Behav. Neurosci. 121, 742–750 (2007).

    Article  PubMed  Google Scholar 

  89. Rodo, C., Sargolini, F. & Save, E. Processing of spatial and non-spatial information in rats with lesions of the medial and lateral entorhinal cortex: Environmental complexity matters. Behav. Brain Res. 320, 200–209 (2017).

    Article  PubMed  Google Scholar 

  90. Kuruvilla, M.V. & Ainge, J.A. Lateral entorhinal cortex lesions impair local spatial frameworks. Front. Syst. Neurosci. 11, 30 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. 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).This paper showed the phenomenon of response suppression in inferomedial temporal cortex, in which neural responses to novel stimuli decrease with repeated exposures.

    Article  CAS  PubMed  Google Scholar 

  92. Fahy, F.L., Riches, I.P. & Brown, M.W. Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp. Brain Res. 96, 457–472 (1993).

    Article  CAS  PubMed  Google Scholar 

  93. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zhu, X.O., Brown, M.W. & Aggleton, J.P. Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur. J. Neurosci. 7, 753–765 (1995).

    Article  CAS  PubMed  Google Scholar 

  95. Wan, H., Aggleton, J.P. & Brown, M.W. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J. Neurosci. 19, 1142–1148 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Young, B.J., Fox, G.D. & Eichenbaum, H. Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J. Neurosci. 14, 6553–6563 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Deshmukh, S.S. & Knierim, J.J. Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 5, 69 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Deshmukh, S.S., Johnson, J.L. & Knierim, J.J. Perirhinal cortex represents nonspatial, but not spatial, information in rats foraging in the presence of objects: comparison with lateral entorhinal cortex. Hippocampus 22, 2045–2058 (2012).

    Article  PubMed  Google Scholar 

  99. Burke, S.N. et al. Representation of three-dimensional objects by the rat perirhinal cortex. Hippocampus 22, 2032–2044 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Tsao, A., Moser, M.B. & Moser, E.I. Traces of experience in the lateral entorhinal cortex. Curr. Biol. 23, 399–405 (2013).

    Article  CAS  PubMed  Google Scholar 

  101. Weible, A.P., Rowland, D.C., Monaghan, C.K., Wolfgang, N.T. & Kentros, C.G. Neural correlates of long-term object memory in the mouse anterior cingulate cortex. J. Neurosci. 32, 5598–5608 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Deshmukh, S.S. & Knierim, J.J. Influence of local objects on hippocampal representations: Landmark vectors and memory. Hippocampus 23, 253–267 (2013).

    Article  PubMed  Google Scholar 

  103. Giocomo, L.M., Moser, M.-B. & Moser, E.I. Computational models of grid cells. Neuron 71, 589–603 (2011).

    Article  CAS  PubMed  Google Scholar 

  104. Aggleton, J.P., Kyd, R.J. & Bilkey, D.K. When is the perirhinal cortex necessary for the performance of spatial memory tasks? Neurosci. Biobehav. Rev. 28, 611–624 (2004).

    Article  PubMed  Google Scholar 

  105. Kealy, J. & Commins, S. The rat perirhinal cortex: a review of anatomy, physiology, plasticity, and function. Prog. Neurobiol. 93, 522–548 (2011).

    Article  CAS  PubMed  Google Scholar 

  106. Ferbinteanu, J., Holsinger, R.M. & McDonald, R.J. Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context. Behav. Brain Res. 101, 65–84 (1999).

    Article  CAS  PubMed  Google Scholar 

  107. Wiig, K.A. & Bilkey, D.K. The effects of perirhinal cortical lesions on spatial reference memory in the rat. Behav. Brain Res. 63, 101–109 (1994).

    Article  CAS  PubMed  Google Scholar 

  108. Burwell, R.D., Saddoris, M.P., Bucci, D.J. & Wiig, K.A. Corticohippocampal contributions to spatial and contextual learning. J. Neurosci. 24, 3826–3836 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Nelson, A.J., Olarte-Sánchez, C.M., Amin, E. & Aggleton, J.P. Perirhinal cortex lesions that impair object recognition memory spare landmark discriminations. Behav. Brain Res. 313, 255–259 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Stranahan, A.M., Salas-Vega, S., Jiam, N.T. & Gallagher, M. Interference with reelin signaling in the lateral entorhinal cortex impairs spatial memory. Neurobiol. Learn. Mem. 96, 150–155 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Burwell, R.D., Shapiro, M.L., O'Malley, M.T. & Eichenbaum, H. Positional firing properties of perirhinal cortex neurons. Neuroreport 9, 3013–3018 (1998).

    Article  CAS  PubMed  Google Scholar 

  112. Hargreaves, E.L., Rao, G., Lee, I. & Knierim, J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308, 1792–1794 (2005).

    Article  CAS  PubMed  Google Scholar 

  113. Yoganarasimha, D., Rao, G. & Knierim, J.J. Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21, 1363–1374 (2011).

    Article  CAS  PubMed  Google Scholar 

  114. Zironi, I., Iacovelli, P., Aicardi, G., Liu, P. & Bilkey, D.K. Prefrontal cortex lesions augment the location-related firing properties of area TE/perirhinal cortex neurons in a working memory task. Cereb. Cortex 11, 1093–1100 (2001).

    Article  CAS  PubMed  Google Scholar 

  115. Deshmukh, S.S., Yoganarasimha, D., Voicu, H. & Knierim, J.J. Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 104, 994–1006 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).

    Article  CAS  PubMed  Google Scholar 

  117. Savelli, F., Luck, J.D. & Knierim, J.J. Framing of grid cells within and beyond navigation boundaries. Elife 6, e21354 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Wiig, K.A. & Bilkey, D.K. Perirhinal cortex lesions in rats disrupt performance in a spatial DNMS task. Neuroreport 5, 1405–1408 (1994).

    CAS  PubMed  Google Scholar 

  119. Wiig, K.A. & Burwell, R.D. Memory impairment on a delayed non-matching-to-position task after lesions of the perirhinal cortex in the rat. Behav. Neurosci. 112, 827–838 (1998).

    Article  CAS  PubMed  Google Scholar 

  120. Liu, P. & Bilkey, D.K. Excitotoxic lesions centered on perirhinal cortex produce delay-dependent deficits in a test of spatial memory. Behav. Neurosci. 112, 512–524 (1998).

    Article  CAS  PubMed  Google Scholar 

  121. Liu, P. & Bilkey, D.K. The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. Behav. Neurosci. 113, 672–682 (1999).

    Article  CAS  PubMed  Google Scholar 

  122. Ennaceur, A., Neave, N. & Aggleton, J.P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav. Brain Res. 80, 9–25 (1996).

    Article  CAS  PubMed  Google Scholar 

  123. Liu, P. & Bilkey, D.K. Lesions of perirhinal cortex produce spatial memory deficits in the radial maze. Hippocampus 8, 114–121 (1998).

    Article  CAS  PubMed  Google Scholar 

  124. Otto, T., Wolf, D. & Walsh, T.J. Combined lesions of perirhinal and entorhinal cortex impair rats' performance in two versions of the spatially guided radial-arm maze. Neurobiol. Learn. Mem. 68, 21–31 (1997).

    Article  CAS  PubMed  Google Scholar 

  125. Bucci, D.J., Phillips, R.G. & Burwell, R.D. Contributions of postrhinal and perirhinal cortex to contextual information processing. Behav. Neurosci. 114, 882–894 (2000).

    Article  CAS  PubMed  Google Scholar 

  126. Bucci, D.J., Saddoris, M.P. & Burwell, R.D. Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behav. Neurosci. 116, 479–488 (2002).

    Article  PubMed  Google Scholar 

  127. Ramos, J.M.J. Perirhinal cortex involvement in allocentric spatial learning in the rat: Evidence from doubly marked tasks. Hippocampus 27, 507–517 (2017).

    Article  PubMed  Google Scholar 

  128. Bos, J.J. et al. Perirhinal firing patterns are sustained across large spatial segments of the task environment. Nat. Commun. 8, 15602 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Collett, T.S., Cartwright, B.A. & Smith, B.A. Landmark learning and visuo-spatial memories in gerbils. J. Comp. Physiol. A 158, 835–851 (1986).This study shows that animals can learn to search for food at locations defined by a vector relationship to individual landmarks.

    Article  CAS  PubMed  Google Scholar 

  130. Biegler, R. & Morris, R.G. Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361, 631–633 (1993).

    Article  CAS  PubMed  Google Scholar 

  131. Neunuebel, J.P., Yoganarasimha, D., Rao, G. & Knierim, J.J. Conflicts between local and global spatial frameworks dissociate neural representations of the lateral and medial entorhinal cortex. J. Neurosci. 33, 9246–9258 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Keene, C.S. et al. Complementary functional organization of neuronal activity patterns in the perirhinal, lateral entorhinal, and medial entorhinal cortices. J. Neurosci. 36, 3660–3675 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Manns, J.R. & Eichenbaum, H. A cognitive map for object memory in the hippocampus. Learn. Mem. 16, 616–624 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Burke, S.N. et al. The influence of objects on place field expression and size in distal hippocampal CA1. Hippocampus 21, 783–801 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Rivard, B., Li, Y., Lenck-Santini, P.P., Poucet, B. & Muller, R.U. Representation of objects in space by two classes of hippocampal pyramidal cells. J. Gen. Physiol. 124, 9–25 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Sarel, A., Finkelstein, A., Las, L. & Ulanovsky, N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355, 176–180 (2017).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Maass, A., Berron, D., Libby, L.A., Ranganath, C. & Düzel, E. Functional subregions of the human entorhinal cortex. Elife 4, 06426 (2015).This study provides evidence for a functional parcellation of the medial and lateral entorhinal cortex in humans, similar to that shown in rodents.

    Article  Google Scholar 

  139. Schultz, H., Sommer, T. & Peters, J. Direct evidence for domain-sensitive functional subregions in human entorhinal cortex. J. Neurosci. 32, 4716–4723 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Reagh, Z.M. & Yassa, M.A. Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans. Proc. Natl. Acad. Sci. USA 111, E4264–E4273 (2014).This paper demonstrates a functional space vs. object dissociation between putative medial and lateral entorhinal cortex regions in the human.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Lisman, J.E. Role of the dual entorhinal inputs to hippocampus: a hypothesis based on cue/action (non-self/self) couplets. Prog. Brain Res. 163, 615–625 (2007).

    Article  PubMed  Google Scholar 

  142. Knierim, J.J., Neunuebel, J.P. & Deshmukh, S.S. Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames. Phil. Trans. R. Soc. Lond. B 369, 20130369 (2013).

    Article  Google Scholar 

  143. Furtak, S.C., Ahmed, O.J. & Burwell, R.D. Single neuron activity and theta modulation in postrhinal cortex during visual object discrimination. Neuron 76, 976–988 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Sereno, A.B. & Lehky, S.R. Population coding of visual space: comparison of spatial representations in dorsal and ventral pathways. Front. Comput. Neurosci. 4, 159 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Kraus, B.J. et al. During running in place, grid cells integrate elapsed time and distance run. Neuron 88, 578–589 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Konen, C.S. & Kastner, S. Two hierarchically organized neural systems for object information in human visual cortex. Nat. Neurosci. 11, 224–231 (2008).

    Article  CAS  PubMed  Google Scholar 

  147. Murata, A., Gallese, V., Luppino, G., Kaseda, M. & Sakata, H. Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J. Neurophysiol. 83, 2580–2601 (2000).

    Article  CAS  PubMed  Google Scholar 

  148. Sereno, A.B. & Maunsell, J.H.R. Shape selectivity in primate lateral intraparietal cortex. Nature 395, 500–503 (1998).

    Article  CAS  PubMed  Google Scholar 

  149. Fitzgerald, J.K., Freedman, D.J. & Assad, J.A. Generalized associative representations in parietal cortex. Nat. Neurosci. 14, 1075–1079 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Burkhalter, A. The network for intracortical communication in mouse visual cortex. in Micro-, Meso-, and Macro-Connectomics of the Brain (eds. Kennedy, H. et al.) (Springer, Cham, Switzerland, 2016).

    Chapter  Google Scholar 

Download references

Acknowledgements

Work from the authors' laboratories was funded by Public Health Service grants EY024028 (C.E.C.), EY011797 (C.E.C.), NS039456 (J.J.K.) and MH094146 (J.J.K.).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Charles E Connor or James J Knierim.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Connor, C., Knierim, J. Integration of objects and space in perception and memory. Nat Neurosci 20, 1493–1503 (2017). https://doi.org/10.1038/nn.4657

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.4657

This article is cited by

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