Emergence of transformation-tolerant representations of visual objects in rat lateral extrastriate cortex

eLife

Volumn 6, Issue , 2017, Pages

  Tafazoli, Sina ^a,d   Safaai, Houman ^a,b,c   De Franceschi, Gioia ^a,e   Rosselli, Federica Bianca ^a,f   Vanzella, Walter ^a   Riggi, Margherita ^a   Buffolo, Federica ^a,b   Panzeri, Stefano ^b   Zoccolan, Davide ^a  

^a SISSA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c HARVARD MEDICAL SCHOOL   (United States)

^d PRINCETON UNIVERSITY   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; BRAIN CORTEX; DISEASE MODEL; IDENTITY; NERVE CELL; NONHUMAN; RAT; RODENT; SPECIALIZATION; STRIATE CORTEX; VISUAL INFORMATION; ANIMAL; PATTERN RECOGNITION; PHYSIOLOGY; VISION; VISUAL CORTEX;

ANIMALS; NEURONS; PATTERN RECOGNITION, VISUAL; RATS; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 85017468101     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.22794     Document Type: Article

References (99)

1. Acharya L, Aghajan ZM, Vuong C, Moore JJ, Mehta MR. 2016. Causal influence of visual cues on hippocampal directional selectivity. Cell 164:197-207. doi: 10.1016/j.cell.2015.12.015, PMID: 26709045
2. Aggleton JP, Keen S, Warburton EC, Bussey TJ. 1997. Extensive cytotoxic lesions involving both the rhinal cortices and area TE impair recognition but spare spatial alternation in the rat. Brain Research Bulletin 43:279-287. doi: 10.1016/S0361-9230(97)00007-5, PMID: 9227838
3. Alemi-Neissi A, Rosselli FB, Zoccolan D. 2013. Multifeatural shape processing in rats engaged in invariant visual object recognition. Journal of Neuroscience 33:5939-5956. doi: 10.1523/JNEUROSCI.3629-12.2013, PMID: 23554476
4. Andermann ML, Kerlin AM, Roumis DK, Glickfeld LL, Reid RC. 2011. Functional specialization of mouse higher visual cortical areas. Neuron 72:1025-1039. doi: 10.1016/j.neuron.2011.11.013, PMID: 22196337
5. Baldassi C, Alemi-Neissi A, Pagan M, Dicarlo JJ, Zecchina R, Zoccolan D. 2013. Shape similarity, better than semantic membership, accounts for the structure of visual object representations in a population of monkey inferotemporal neurons. PLoS Computational Biology 9:e1003167. doi: 10.1371/journal.pcbi.1003167, PMID: 23950700
6. Blanche TJ, Spacek MA, Hetke JF, Swindale NV. 2005. Polytrodes: high-density silicon electrode arrays for large- scale multiunit recording. Journal of Neurophysiology 93:2987-3000. doi: 10.1152/jn.01023.2004, PMID: 1554 8620
7. Borst A, Theunissen FE. 1999. Information theory and neural coding. Nature Neuroscience 2:947-957. doi: 10. 1038/14731, PMID: 10526332
8. Brincat SL, Connor CE. 2004. Underlying principles of visual shape selectivity in posterior inferotemporal cortex. Nature Neuroscience 7:880-886. doi: 10.1038/nn1278, PMID: 15235606
9. Burgess CR, Ramesh RN, Sugden AU, Levandowski KM, Minnig MA, Fenselau H, Lowell BB, Andermann ML. 2016. Hunger-Dependent enhancement of food cue responses in mouse postrhinal cortex and lateral amygdala. Neuron 91:1154-1169. doi: 10.1016/j.neuron.2016.07.032, PMID: 27523426
10. Busse L, Wade AR, Carandini M. 2009. Representation of concurrent stimuli by population activity in visual cortex. Neuron 64:931-942. doi: 10.1016/j.neuron.2009.11.004, PMID: 20064398
11. Chen YP, Lin CP, Hsu YC, Hung CP. 2015. Network anisotropy trumps noise for efficient object coding in macaque inferior temporal cortex. Journal of Neuroscience 35:9889-9899. doi: 10.1523/JNEUROSCI.4595-14. 2015, PMID: 26156990
12. Coogan TA, Burkhalter A. 1993. Hierarchical organization of areas in rat visual cortex. Journal of Neuroscience 13:3749-3772. PMID: 7690066
13. Cooke SF, Bear MF. 2015. Visual recognition memory: a view from V1. Current Opinion in Neurobiology 35:57-65. doi: 10.1016/j.conb.2015.06.008, PMID: 26151761
14. Cover TM, Thomas JA. 2006. 2nd Edn. Elements of Information Theory. Hoboken, N.J: Wiley-Interscience.
15. Cristianini N, Shawe-Taylor J. 2000. An Introduction to Support Vector Machines: And Other Kernel-Based Learning Methods. New York, NY, USA: Cambridge University Press.
16. Cushman JD, Aharoni DB, Willers B, Ravassard P, Kees A, Vuong C, Popeney B, Arisaka K, Mehta MR. 2013. Multisensory control of multimodal behavior: do the legs know what the tongue is doing? PLoS One 8:e80465. doi: 10.1371/journal.pone.0080465, PMID: 24224054
17. DiCarlo JJ, Lane JW, Hsiao SS, Johnson KO. 1996. Marking microelectrode penetrations with fluorescent dyes. Journal of Neuroscience Methods 64:75-81. doi: 10.1016/0165-0270(95)00113-1, PMID: 8869487
18. DiCarlo JJ, Zoccolan D, Rust NC. 2012. How does the brain solve visual object recognition? Neuron 73:415-434. doi: 10.1016/j.neuron.2012.01.010, PMID: 22325196
19. El-Shamayleh Y, Pasupathy A. 2016. Contour curvature as an invariant code for objects in visual area V4. Journal of Neuroscience 36:5532-5543. doi: 10.1523/JNEUROSCI.4139-15.2016, PMID: 27194333
20. Espinoza SG, Thomas HC. 1983. Retinotopic organization of striate and extrastriate visual cortex in the hooded rat. Brain Research 272:137-144. doi: 10.1016/0006-8993(83)90370-0, PMID: 6616189
21. Fabre-Thorpe M, Richard G, Thorpe SJ. 1998. Rapid categorization of natural images by rhesus monkeys. NeuroReport 9:303-308. doi: 10.1097/00001756-199801260-00023, PMID: 9507973
22. Froudarakis E, Berens P, Ecker AS, Cotton RJ, Sinz FH, Yatsenko D, Saggau P, Bethge M, Tolias AS. 2014.
23. Population code in mouse V1 facilitates readout of natural scenes through increased sparseness. Nature Neuroscience 17:851-857. doi: 10.1038/nn.3707, PMID: 24747577
24. Gallardo L, Mottles M, Vera L, Carrasco MA, Torrealba F, Montero VM, Pinto-Hamuy T. 1979. Failure by rats to learn a visual conditional discrimination after lateral peristriate cortical lesions. Physiological Psychology 7:173-177. doi: 10.3758/BF03332905
25. Gavornik JP, Bear MF. 2014. Higher brain functions served by the lowly rodent primary visual cortex. Learning & Memory 21:527-533. doi: 10.1101/lm.034355.114, PMID: 25225298
26. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I. 2008. Internally generated reactivation of single neurons in human Hippocampus during free recall. Science 322:96-101. doi: 10.1126/science.1164685, PMID: 1 8772395
27. Glickfeld LL, Reid RC, Andermann ML. 2014. A mouse model of higher visual cortical function. Current Opinion in Neurobiology 24:28-33. doi: 10.1016/j.conb.2013.08.009, PMID: 24492075
28. Haider B, Häusser M, Carandini M. 2013. Inhibition dominates sensory responses in the awake cortex. Nature 493:97-100. doi: 10.1038/nature11665, PMID: 23172139
29. Hastie T, Tibshirani R, Friedman J. 2009. The Elements of Statistical Learning: Data Mining, Inference, and Prediction 2 Edizione. Springer-Verlag.
30. Heinke W, Schwarzbauer C. 2001. Subanesthetic isoflurane affects task-induced brain activation in a highly specific manner: a functional magnetic resonance imaging study. Anesthesiology 94:973-981. doi: 10.1097/00000542-200106000-00010, PMID: 11465623
31. Hill DN, Mehta SB, Kleinfeld D. 2011. Quality metrics to accompany spike sorting of extracellular signals. Journal of Neuroscience 31:8699-8705. doi: 10.1523/JNEUROSCI.0971-11.2011, PMID: 21677152
32. Hong H, Yamins DL, Majaj NJ, DiCarlo JJ. 2016. Explicit information for category-orthogonal object properties increases along the ventral stream. Nature Neuroscience 19:613-622. doi: 10.1038/nn.4247, PMID: 26900926
33. Huberman AD, Niell CM. 2011. What can mice tell Us about how vision works? Trends in Neurosciences 34:464-473. doi: 10.1016/j.tins.2011.07.002, PMID: 21840069
34. Hung CP, Kreiman G, Poggio T, DiCarlo JJ. 2005. Fast readout of object identity from macaque inferior temporal cortex. Science 310:863-866. doi: 10.1126/science.1117593, PMID: 16272124
35. Ince RA, Mazzoni A, Bartels A, Logothetis NK, Panzeri S. 2012. A novel test to determine the significance of neural selectivity to single and multiple potentially correlated stimulus features. Journal of Neuroscience Methods 210:49-65. doi: 10.1016/j.jneumeth.2011.11.013, PMID: 22142889
36. Ito M, Tamura H, Fujita I, Tanaka K. 1995. Size and position invariance of neuronal responses in monkey inferotemporal cortex. Journal of Neurophysiology 73:218-226. PMID: 7714567
37. Juavinett AL, Callaway EM. 2015. Pattern and component motion responses in mouse visual cortical areas. Current Biology: CB 25:1759-1764. doi: 10.1016/j.cub.2015.05.028, PMID: 26073133
38. Katzner S, Weigelt S. 2013. Visual cortical networks: of mice and men. Current Opinion in Neurobiology 23:202-206. doi: 10.1016/j.conb.2013.01.019, PMID: 23415830
39. Kiani R, Esteky H, Mirpour K, Tanaka K. 2007. Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. Journal of Neurophysiology 97:4296-4309. doi: 10.1152/jn. 00024.2007, PMID: 17428910
40. Kobatake E, Tanaka K. 1994. Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. Journal of Neurophysiology 71:856-867. PMID: 8201425
41. Li N, Cox DD, Zoccolan D, DiCarlo JJ. 2009. What response properties do individual neurons need to underlie position and clutter “invariant” object recognition? Journal of Neurophysiology 102:360-376. doi: 10.1152/jn. 90745.2008, PMID: 19439676
42. Logothetis NK, Guggenberger H, Peled S, Pauls J. 1999. Functional imaging of the monkey brain. Nature Neuroscience 2:555-562. doi: 10.1038/9210, PMID: 10448221
43. Luo L, Callaway EM, Svoboda K. 2008. Genetic dissection of neural circuits. Neuron 57:634-660. doi: 10.1016/j. neuron.2008.01.002, PMID: 18341986
44. Magri C, Whittingstall K, Singh V, Logothetis NK, Panzeri S. 2009. A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings. BMC Neuroscience 10:81. doi: 10.1186/1471-2202-10-81, PMID: 19607698
45. Marshel JH, Garrett ME, Nauhaus I, Callaway EM. 2011. Functional specialization of seven mouse visual cortical areas. Neuron 72:1040-1054. doi: 10.1016/j.neuron.2011.12.004, PMID: 22196338
46. McDaniel WF, Coleman J, Lindsay JF. 1982. A comparison of lateral peristriate and striate neocortical ablations in the rat. Behavioural Brain Research 6:249-272. doi: 10.1016/0166-4328(82)90027-4, PMID: 7171386
47. Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S. 2008. Phase-of-firing coding of natural visual stimuli in primary visual cortex. Current Biology: CB 18:375-380. doi: 10.1016/j.cub.2008.02.023, PMID: 18328702
48. Montero VM. 1993. Retinotopy of cortical connections between the striate cortex and extrastriate visual areas in the rat. Experimental Brain Research 94:1-15. doi: 10.1007/BF00230466, PMID: 8335065
49. Nandy AS, Sharpee TO, Reynolds JH, Mitchell JF. 2013. The fine structure of shape tuning in area V4. Neuron 78:1102-1115. doi: 10.1016/j.neuron.2013.04.016, PMID: 23791199
50. Niell CM, Stryker MP. 2008. Highly selective receptive fields in mouse visual cortex. Journal of Neuroscience 28:7520-7536. doi: 10.1523/JNEUROSCI.0623-08.2008, PMID: 18650330
51. Niell CM, Stryker MP. 2010. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:472-479. doi: 10.1016/j.neuron.2010.01.033, PMID: 20188652
52. Niell CM. 2011. Exploring the next frontier of mouse vision. Neuron 72:889-892. doi: 10.1016/j.neuron.2011.12. 011, PMID: 22196324
53. Op De Beeck H, Vogels R. 2000. Spatial sensitivity of macaque inferior temporal neurons. The Journal of Comparative Neurology 426:505-518. doi: 10.1002/1096-9861(20001030)426:4<505::AID-CNE1>3.0.CO;2-M, PMID: 11027395
54. Optican LM, Richmond BJ. 1987. Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. information theoretic analysis. Journal of Neurophysiology 57:162-178. PMID: 355 9670
55. Pagan M, Urban LS, Wohl MP, Rust NC. 2013. Signals in inferotemporal and perirhinal cortex suggest an untangling of visual target information. Nature Neuroscience 16:1132-1139. doi: 10.1038/nn.3433, PMID: 237 92943
56. Panzeri S, Treves A. 1996. Analytical estimates of limited sampling biases in different information measures. Network 7:87-107. doi: 10.1088/0954-898X/7/1/006
57. Panzeri S, Senatore R, Montemurro MA, Petersen RS. 2007. Correcting for the sampling Bias problem in spike train information measures. Journal of Neurophysiology 98:1064-1072. doi: 10.1152/jn.00559.2007, PMID: 17615128
58. Pasupathy A, Connor CE. 2002. Population coding of shape in area V4. Nature Neuroscience 5:1332-1338. doi: 10.1038/nn972, PMID: 12426571
59. Pecka M, Han Y, Sader E, Mrsic-Flogel TD. 2014. Experience-dependent specialization of receptive field surround for selective coding of natural scenes. Neuron 84:457-469. doi: 10.1016/j.neuron.2014.09.010, PMID: 25263755
60. Polack PO, Contreras D. 2012. Long-range parallel processing and local recurrent activity in the visual cortex of the mouse. Journal of Neuroscience 32:11120-11131. doi: 10.1523/JNEUROSCI.6304-11.2012, PMID: 22875 943
61. Quian Quiroga R, Panzeri S. 2009. Extracting information from neuronal populations: information theory and decoding approaches. Nature Reviews. Neuroscience 10:173-185. doi: 10.1038/nrn2578, PMID: 19229240
62. Quiroga RQ, Nadasdy Z, Ben-Shaul Y. 2004. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Computation 16:1661-1687. doi: 10.1162/089976604774201631, PMID: 15228749
63. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. 2005. Invariant visual representation by single neurons in the human brain. Nature 435:1102-1107. doi: 10.1038/nature03687, PMID: 15973409
64. Quiroga RQ, Mukamel R, Isham EA, Malach R, Fried I. 2008. Human single-neuron responses at the threshold of conscious recognition. PNAS 105:3599-3604. doi: 10.1073/pnas.0707043105, PMID: 18299568
65. Rieke F, Warland D, Ruyter van Steveninck RR, Bialek W. 1997. Spikes: Exploring the Neural Code. Cambridge, MA: MIT Press.
66. Rolls ET, Tovee MJ. 1995. Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. Journal of Neurophysiology 73:713-726. PMID: 7760130
67. Rolls ET, Treves A. 2011. The neuronal encoding of information in the brain. Progress in Neurobiology 95:448-490. doi: 10.1016/j.pneurobio.2011.08.002, PMID: 21907758
68. Rosselli FB, Alemi A, Ansuini A, Zoccolan D. 2015. Object similarity affects the perceptual strategy underlying invariant visual object recognition in rats. Frontiers in Neural Circuits 9:10. doi: 10.3389/fncir.2015.00010, PMID: 25814936
69. Rousselet GA, Fabre-Thorpe M, Thorpe SJ. 2002. Parallel processing in high-level categorization of natural images. Nature Neuroscience 5:629-630. doi: 10.1038/nn866, PMID: 12032544
70. Rust NC, Dicarlo JJ. 2010. Selectivity and tolerance (“invariance”) both increase as visual information propagates from cortical area V4 to IT. Journal of Neuroscience 30:12978-12995. doi: 10.1523/JNEUROSCI.0179-10.2010, PMID: 20881116
71. Rust NC, DiCarlo JJ. 2012. Balanced increases in selectivity and tolerance produce constant sparseness along the ventral visual stream. Journal of Neuroscience 32:10170-10182. doi: 10.1523/JNEUROSCI.6125-11.2012, PMID: 22836252
72. Sanderson KJ, Dreher B, Gayer N. 1991. Prosencephalic connections of striate and extrastriate areas of rat visual cortex. Experimental Brain Research 85:324-334. doi: 10.1007/BF00229410, PMID: 1716594
73. Sato T, Uchida G, Lescroart MD, Kitazono J, Okada M, Tanifuji M. 2013. Object representation in inferior temporal cortex is organized hierarchically in a mosaic-like structure. Journal of Neuroscience 33:16642-16656. doi: 10.1523/JNEUROSCI.5557-12.2013, PMID: 24133267
74. Schuett S, Bonhoeffer T, Hübener M. 2002. Mapping retinotopic structure in mouse visual cortex with optical imaging. Journal of Neuroscience 22:6549-6559. PMID: 12151534
75. Schölkopf B, Smola AJ. 2001. Learning with Kernels. MIT Press.
76. Sharpee TO, Kouh M, Reynolds JH. 2013. Trade-off between curvature tuning and position invariance in visual area V4. PNAS 110:11618-11623. doi: 10.1073/pnas.1217479110, PMID: 23798444
77. Steriade M, Nuñez A, Amzica F. 1993. A novel slow (< 1 hz) oscillation of neocortical neurons in vivo:depolarizing and hyperpolarizing components. Journal of Neuroscience 13:3252-3265. PMID: 8340806
78. Sugase Y, Yamane S, Ueno S, Kawano K. 1999. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400:869-873. doi: 10.1038/23703, PMID: 10476965
79. Sánchez RF, Montero VM, Espinoza SG, Díaz E, Canitrot M, Pinto-Hamuy T. 1997. Visuospatial discrimination deficit in rats after ibotenate lesions in anteromedial visual cortex. Physiology & Behavior 62:989-994. doi: 10. 1016/S0031-9384(97)00201-1, PMID: 9333191
80. Tafazoli S, Di Filippo A, Zoccolan D. 2012. Transformation-tolerant object recognition in rats revealed by visual priming. Journal of Neuroscience 32:21-34. doi: 10.1523/JNEUROSCI.3932-11.2012, PMID: 22219267
81. Tees RC. 1999. The effects of posterior parietal and posterior temporal cortical lesions on multimodal spatial and nonspatial competencies in rats. Behavioural Brain Research 106:55-73. doi: 10.1016/S0166-4328(99)00092-3, PMID: 10595422
82. Thorpe S, Fize D, Marlot C. 1996. Speed of processing in the human visual system. Nature 381:520-522. doi: 10. 1038/381520a0, PMID: 8632824
83. Tovee MJ, Rolls ET, Azzopardi P. 1994. Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. Journal of Neurophysiology 72:1049-1060. PMID: 7807195
84. Tsunoda K, Yamane Y, Nishizaki M, Tanifuji M. 2001. Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nature Neuroscience 4:832-838. doi: 10.1038/90547, PMID: 11477430
85. Vaiceliunaite A, Erisken S, Franzen F, Katzner S, Busse L. 2013. Spatial integration in mouse primary visual cortex. Journal of Neurophysiology 110:964-972. doi: 10.1152/jn.00138.2013, PMID: 23719206
86. Vermaercke B, Op de Beeck HP. 2012. A multivariate approach reveals the behavioral templates underlying visual discrimination in rats. Current Biology: CB 22:50-55. doi: 10.1016/j.cub.2011.11.041, PMID: 22209530
87. Vermaercke B, Gerich FJ, Ytebrouck E, Arckens L, Op de Beeck HP, Van den Bergh G. 2014. Functional specialization in rat occipital and temporal visual cortex. Journal of Neurophysiology 112:1963-1983. doi: 10. 1152/jn.00737.2013, PMID: 24990566
88. Vinje WE, Gallant JL. 2000. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276. doi: 10.1126/science.287.5456.1273, PMID: 10678835
89. Vinken K, Vermaercke B, Op de Beeck HP. 2014. Visual categorization of natural movies by rats. Journal of Neuroscience 34:10645-10658. doi: 10.1523/JNEUROSCI.3663-13.2014, PMID: 25100598
90. Wang Q, Burkhalter A. 2007. Area map of mouse visual cortex. The Journal of Comparative Neurology 502:339-357. doi: 10.1002/cne.21286, PMID: 17366604
91. Wang Q, Gao E, Burkhalter A. 2011. Gateways of ventral and dorsal streams in mouse visual cortex. Journal of Neuroscience 31:1905-1918. doi: 10.1523/JNEUROSCI.3488-10.2011, PMID: 21289200
92. Wang Q, Sporns O, Burkhalter A. 2012. Network analysis of corticocortical connections reveals ventral and dorsal processing streams in mouse visual cortex. Journal of Neuroscience 32:4386-4399. doi: 10.1523/JNEUROSCI. 6063-11.2012, PMID: 22457489
93. Wiesenfeld Z, Branchek T. 1976. Refractive state and visual acuity in the hooded rat. Vision Research 16:823-827. doi: 10.1016/0042-6989(76)90142-5, PMID: 960609
94. Willmore BD, Prenger RJ, Gallant JL. 2010. Neural representation of natural images in visual area V2. Journal of Neuroscience 30:2102-2114. doi: 10.1523/JNEUROSCI.4099-09.2010, PMID: 20147538
95. Wörtwein G, Mogensen J, Williams G, Carlos JH, Divac I. 1994. Cortical area in the rat that mediates visual pattern discrimination. Acta Neurobiologiae Experimentalis 54:365-376. PMID: 7887187
96. Zhu Y, Yao H. 2013. Modification of visual cortical receptive field induced by natural stimuli. Cerebral Cortex 23:1923-1932. doi: 10.1093/cercor/bhs178, PMID: 22735159
97. Zoccolan D, Kouh M, Poggio T, DiCarlo JJ. 2007. Trade-off between object selectivity and tolerance in monkey inferotemporal cortex. Journal of Neuroscience 27:12292-12307. doi: 10.1523/JNEUROSCI.1897-07.2007, PMID: 17989294
98. Zoccolan D, Oertelt N, DiCarlo JJ, Cox DD. 2009. A rodent model for the study of invariant visual object recognition. PNAS 106:8748-8753. doi: 10.1073/pnas.0811583106, PMID: 19429704
99. Zoccolan D. 2015. Invariant visual object recognition and shape processing in rats. Behavioural Brain Research 285:10-33. doi: 10.1016/j.bbr.2014.12.053, PMID: 25561421