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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: 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.

References

  1. 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.

  2. 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).

  3. 3

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

  4. 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).

  5. 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).

  6. 6

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

  7. 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.

  8. 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.

  9. 9

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

  10. 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.

  11. 11

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

  12. 12

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

  13. 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).

  14. 14

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

  15. 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).

  16. 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).

  17. 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.

  18. 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).

  19. 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).

  20. 20

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

  21. 21

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

  22. 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).

  23. 23

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

  24. 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).

  25. 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).

  26. 26

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

  27. 27

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

  28. 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).

  29. 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).

  30. 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).

  31. 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).

  32. 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).

  33. 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).

  34. 34

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

  35. 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).

  36. 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).

  37. 37

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

  38. 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).

  39. 39

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

  40. 40

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

  41. 41

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

  42. 42

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

  43. 43

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

  44. 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).

  45. 45

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

  46. 46

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

  47. 47

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

  48. 48

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

  49. 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).

  50. 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).

  51. 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).

  52. 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).

  53. 53

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

  54. 54

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

  55. 55

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

  56. 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.

  57. 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).

  58. 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).

  59. 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.

  60. 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.

  61. 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.

  62. 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).

  63. 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.

  64. 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.

  65. 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.

  66. 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).

  67. 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).

  68. 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).

  69. 69

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

  70. 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.

  71. 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.

  72. 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).

  73. 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.

  74. 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).

  75. 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.

  76. 76

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

  77. 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).

  78. 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).

  79. 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).

  80. 80

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

  81. 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).

  82. 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).

  83. 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).

  84. 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).

  85. 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).

  86. 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).

  87. 87

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

  88. 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).

  89. 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).

  90. 90

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

  91. 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.

  92. 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).

  93. 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).

  94. 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).

  95. 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).

  96. 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).

  97. 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).

  98. 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).

  99. 99

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

  100. 100

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

  101. 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).

  102. 102

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

  103. 103

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

  104. 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).

  105. 105

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

  106. 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).

  107. 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).

  108. 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).

  109. 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).

  110. 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).

  111. 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).

  112. 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).

  113. 113

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

  114. 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).

  115. 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).

  116. 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).

  117. 117

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

  118. 118

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

  119. 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).

  120. 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).

  121. 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).

  122. 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).

  123. 123

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

  124. 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).

  125. 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).

  126. 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).

  127. 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).

  128. 128

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

  129. 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.

  130. 130

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

  131. 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).

  132. 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).

  133. 133

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

  134. 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).

  135. 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).

  136. 136

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

  137. 137

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

  138. 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.

  139. 139

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

  140. 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.

  141. 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).

  142. 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).

  143. 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).

  144. 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).

  145. 145

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

  146. 146

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

  147. 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).

  148. 148

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

  149. 149

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

  150. 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).

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

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

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

Further reading