Higher brain functions served by the lowly rodent primary visual cortex

Learning and Memory

Volumn 21, Issue 10, 2014, Pages 527-533

  Gavornik, Jeffrey P ^a   Bear, Mark F ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN FUNCTION; BRAIN REGION; EYE DOMINANCE; HUMAN; MEMORY; MONOCULAR DEPRIVATION; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; REVIEW; RODENT; SENSORY CORTEX; STIMULUS RESPONSE; STRIATE CORTEX; ANIMAL; MOUSE; PATTERN RECOGNITION; PHYSIOLOGY; RAT; RECOGNITION; REWARD; VISUAL CORTEX;

ANIMALS; MICE; NEURONAL PLASTICITY; PATTERN RECOGNITION, VISUAL; RATS; RECOGNITION (PSYCHOLOGY); REWARD; VISUAL CORTEX;

EID: 84907727743     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.034355.114     Document Type: Review

References (116)

1. Alink A, Schwiedrzik CM, Kohler A, Singer W, Muckli L. 2010. Stimulus predictability reduces responses in primary visual cortex. J Neurosci 30: 2960-2966.
2. Ayaz A, Saleem AB, Scholvinck ML, Carandini M. 2013. Locomotion controls spatial integration in mouse visual cortex. Curr Biol 23: 890-894.
3. Bach-y-Rita P, Kercel SW. 2003. Sensory substitution and the human-machine interface. Trends Cogn Sci 7: 541-546.
4. Balas B, Sinha P. 2008. Observing object motion induces increased generalization and sensitivity. Perception 37: 1160-1174.
5. Balas BJ, Sinha P. 2009. The role of sequence order in determining view canonicality for novel wire-frame objects. Atten Percept Psychophys 71: 712-723.
6. Bao M, Yang L, Rios C, He B, Engel SA. 2010. Perceptual learning increases the strength of the earliest signals in visual cortex. J Neurosci 30: 15080-15084.
7. Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ. 2012. Canonical microcircuits for predictive coding. Neuron 76: 695-711.
8. Cajal SR. 1899. Comparative study of the sensory areas of the human cortex. In Clark University, 1889-1899: decennial celebration (ed. Story WE), pp. 311-382. Clark University Press, Worcestor, MA.
9. Cajal SR. 1906. Santiago Ramon y Cajal - Nobel lecture: the Structure and connexions of neurons. Vol. 2014. Nobel Media AB 2013, Nobelprize.org.
10. Carandini M, Heeger DJ. 2012. Normalization as a canonical neural computation. Nat Rev Neurosci 13: 51-62.
11. Casanova MF. 2013. Canonical circuits of the cerebral cortex as enablers of neuroprosthetics. Front Syst Neurosci 7: 77.
12. Chubykin AA, Roach EB, Bear MF, Shuler MG. 2013. A cholinergic mechanism for reward timing within primary visual cortex. Neuron 77: 723-735.
13. Clancy KB, Koralek AC, Costa RM, Feldman DE, Carmena JM. 2014. Volitional modulation of optically recorded calcium signals during neuroprosthetic learning. Nat Neurosci 17: 807-809.
14. Cooke SF, Bear MF. 2010. Visual experience induces long-term potentiation in the primary visual cortex. J Neurosci 30: 16304-16313.
15. Cooke SF, Bear MF. 2012. Stimulus-selective response plasticity in the visual cortex: an assay for the assessment of pathophysiology and treatment of cognitive impairment associated with psychiatric disorders. Biol Psychiatry 71: 487-495.
16. Cooke SF, Bear MF. 2014. How the mechanisms of long-term synaptic potentiation and depression serve experience-dependent plasticity in primary visual cortex. Philos Trans R Soc Lond B Biol Sci 369: 20130284.
17. Cox DD, Meier P, Oertelt N, DiCarlo JJ. 2005. 'Breaking' position-invariant object recognition. Nat Neurosci 8: 1145-1147.
18. Creutzfeldt OD. 1977. Generality of the functional structure of the neocortex. Naturwissenschaften 64: 507-517.
19. DiCarlo JJ, Zoccolan D, Rust NC. 2012. How does the brain solve visual object recognition? Neuron 73: 415-434.
20. Domenici L, Parisi V, Maffei L. 1992. Exogenous supply of nerve growth factor prevents the effects of strabismus in the rat. Neuroscience 51: 19-24.
21. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419-451.
22. Douglas RJ, Martin KA. 2007. Mapping the matrix: the ways of neocortex. Neuron 56: 226-238.
23. Douglas RJ, Martin KAC, Whitteridge D. 1989. A canonical microcircuit for neocortex. Neural Comput 1: 480-488.
24. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. 2002. Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178.
25. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L. 1994. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34: 709-720.
26. Fahle M. 2004. Perceptual learning: a case for early selection. J Vis 4: 879-890.
27. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1: 1-47.
28. Frenkel MY, Bear MF. 2004. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44: 917-923.
29. Frenkel MY, Sawtell NB, Diogo AC, Yoon B, Neve RL, Bear MF. 2006. Instructive effect of visual experience in mouse visual cortex. Neuron 51: 339-349.
30. Friston K. 2005. A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 360: 815-836.
31. Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP, Nicoll RA, Huang ZJ, Stryker MP. 2014. A cortical circuit for gain control by behavioral state. Cell 156: 1139-1152.
32. Fuster JM, Jervey JP. 1981. Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. Science 212: 952-955.
33. Gavornik JP, Bear MF. 2014. Learned spatiotemporal sequence recognition and prediction in primary visual cortex. Nat Neurosci 17: 732-737.
34. Gavornik JP, Shouval HZ. 2011. A network of spiking neurons that can represent interval timing: mean field analysis. J Comput Neurosci 30: 501-513.
35. Gavornik JP, Shuler MG, Loewenstein Y, Bear MF, Shouval HZ. 2009. Learning reward timing in cortex through reward dependent expression of synaptic plasticity. Proc Natl Acad Sci 106: 6826-6831.
36. Gilbert CD, Li W. 2012. Adult visual cortical plasticity. Neuron 75: 250-264.
37. Gordon JA, Stryker MP. 1996. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16: 3274-3286.
38. Guo K, Robertson RG, Pulgarin M, Nevado A, Panzeri S, Thiele A, Young MP. 2007. Spatio-temporal prediction and inference by V1 neurons. Eur J Neurosci 26: 1045-1054.
39. Hamilton RH, Pascual-Leone A. 1998. Cortical plasticity associated with Braille learning. Trends Cogn Sci 2: 168-174.
40. Hasan MT, Hernandez-Gonzalez S, Dogbevia G, Trevino M, Bertocchi I, Gruart A, Delgado-Garcia JM. 2013. Role of motor cortex NMDA receptors in learning-dependent synaptic plasticity of behaving mice. Nat Commun 4: 2258.
41. Hasselmo ME. 2006. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16: 710-715.
42. Hawkins J, Blakeslee S. 2004. On intelligence. Times Books, New York.
43. Hill SL, Wang Y, Riachi I, Schurmann F, Markram H. 2012. Statistical connectivity provides a sufficient foundation for specific functional connectivity in neocortical neural microcircuits. Proc Natl Acad Sci 109: E2885-E2894.
44. Hochstein S, Ahissar M. 2002. View from the top: hierarchies and reverse hierarchies in the visual system. Neuron 36: 791-804.
45. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M. 2006. Lifelong learning: ocular dominance plasticity in mouse visual cortex. Curr Opin Neurobiol 16: 451-459.
46. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S. 1999. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98: 739-755.
47. Hubel DH. 1957. Tungsten microelectrode for recording from single units. Science 125: 549-550.
48. Hubel DH, Wiesel TN. 1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160: 106-154.
49. Hubel DH, Wiesel TN. 1968. Receptive fields and functional architecture of monkey striate cortex. J Physiol 195: 215-243.
50. Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206: 419-436.
51. Hubel DH, Wiesel TN, LeVay S. 1976. Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harb Symp Quant Biol 40: 581-589.
52. Jehee JF, Ling S, Swisher JD, van Bergen RS, Tong F. 2012. Perceptual learning selectively refines orientation representations in early visual cortex. J Neurosci 32: 16747-16753.
53. Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N. 1990. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248: 229-231.
54. Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hubener M. 2008. Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat Neurosci 11: 1162-1167.
55. Ko H, Hofer SB, Pichler B, Buchanan KA, Sjostrom PJ, Mrsic-Flogel TD. 2011. Functional specificity of local synaptic connections in neocortical networks. Nature 473: 87-91.
56. Komura Y, Tamura R, Uwano T, Nishijo H, Kaga K, Ono T. 2001. Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature 412: 546-549.
57. Kouh M, Poggio T. 2008. A canonical neural circuit for cortical nonlinear operations. Neural Comput 20: 1427-1451.
58. Krupa DJ, Wiest MC, Shuler MG, Laubach M, Nicolelis MA. 2004. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304: 1989-1992.
59. Le QV. 2013. Building high-level features using large scale unsupervised learning. In 2013 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP), pp. 8595-8598. IEEE.
60. Lee TS, Mumford D. 2003. Hierarchical Bayesian inference in the visual cortex. J Opt Soc Am A Opt Image Sci Vis 20: 1434-1448.
61. Leon MI, Shadlen MN. 2003. Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38: 317-327.
62. Li W. 2014. Learning to smell danger: acquired associative representation of threat in the olfactory cortex. Front Behav Neurosci 8: 98.
63. Li N, DiCarlo JJ. 2008. Unsupervised natural experience rapidly alters invariant object representation in visual cortex. Science 321: 1502-1507.
64. Matthies U, Balog J, Lehmann K. 2013. Temporally coherent visual stimuli boost ocular dominance plasticity. J Neurosci 33: 11774-11778.
65. Mountcastle VB. 1978. An organizing principle for cerebral function: the unit model and the distributed system. In The mindful brain: cortical organization and the group-selective theory of higher brain function (ed. Edelman GM, Mountcastle VB), p. 100. MIT Press, Cambridge.
66. Muckli L, Kohler A, Kriegeskorte N, Singer W. 2005. Primary visual cortex activity along the apparent-motion trace reflects illusory perception. PLoS Biol 3: e265.
67. Newell FN, Wallraven C, Huber S. 2004. The role of characteristic motion in object categorization. J Vis 4: 118-129.
68. Newton JR, Sur M. 2005. Rewiring cortex: functional plasticity of the auditory cortex during development. Plasticity and signal representation in the auditory system, pp. 127-137.
69. Niell CM, Stryker MP. 2008. Highly selective receptive fields in mouse visual cortex. J Neurosci 28: 7520-7536.
70. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433: 597-603.
71. Papadopoulos GC, Parnavelas JG, Buijs RM. 1989. Light and electron microscopic immunocytochemical analysis of the noradrenaline innervation of the rat visual cortex. J Neurocytol 18: 1-10.
72. Patel GH, Kaplan DM, Snyder LH. 2014. Topographic organization in the brain: searching for general principles. Trends Cogn Sci 18: 351-363.
73. Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC, Lee SH, Harrison TC, Feng G, Dan Y. 2013. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16: 1857-1863.
74. Porciatti V, Pizzorusso T, Maffei L. 1999. The visual physiology of the wild type mouse determined with pattern VEPs. Vision Res 39: 3071-3081.
75. Pourtois G, Rauss KS, Vuilleumier P, Schwartz S. 2008. Effects of perceptual learning on primary visual cortex activity in humans. Vision Res 48: 55-62.
76. Purves D, Lotto RB. 2011. Why we see what we do redux: a wholly empirical theory of vision. Sinauer Associates, Sunderland, MA.
77. Rao RP, Ballard DH. 1997. Dynamic model of visual recognition predicts neural response properties in the visual cortex. Neural Comput 9: 721-763.
78. Rao RP, Ballard DH. 1999. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2: 79-87.
79. Riesenhuber M, Poggio T. 1999. Hierarchical models of object recognition in cortex. Nat Neurosci 2: 1019-1025.
80. Rokem A, Silver MA. 2013. The benefits of cholinergic enhancement during perceptual learning are long-lasting. Front Comput Neurosci 7: 66.
81. Sale A, De Pasquale R, Bonaccorsi J, Pietra G, Olivieri D, Berardi N, Maffei L. 2011. Visual perceptual learning induces long-term potentiation in the visual cortex. Neuroscience 172: 219-225.
82. Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF. 2003. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38: 977-985.
83. Schlaggar BL, O'Leary DD. 1991. Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science 252: 1556-1560.
84. Schoups A, Vogels R, Qian N, Orban G. 2001. Practising orientation identification improves orientation coding in V1 neurons. Nature 412: 549-553.
85. Schultz W. 1998. Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27.
86. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275: 1593-1599.
87. Seitz AR, Nanez JE, Holloway SR, Koyama S, Watanabe T. 2005. Seeing what is not there shows the costs of perceptual learning. Proc Natl Acad Sci 102: 9080-9085.
88. Serences JT. 2008. Value-based modulations inhuman visual cortex. Neuron 60: 1169-1181.
89. Serre T, Oliva A, Poggio T. 2007. A feedforward architecture accounts for rapid categorization. Proc Natl Acad Sci 104: 6424-6429.
90. Shouval HZ, Agarwal A, Gavornik JP. 2013. Scaling of perceptual errors can predict the shape of neural tuning curves. Phys Rev Lett 110: 168102.
91. Shouval HZ, Hussain Shuler MG, Shouval AA, Gavornik JP. 2014. What does scalar timing tell us about neural dynamics? Front Hum Neurosci 8.
92. Shuler MG, Bear MF. 2006. Reward timing in the primary visual cortex. Science 311: 1606-1609.
93. Smith SL, Hausser M. 2010. Parallel processing of visual space by neighboring neurons in mouse visual cortex. Nat Neurosci 13: 1144-1149.
94. Spemann H, Mangold H. 2001. Induction of embryonic primordia by implantation of organizers from a different species. 1923. Int J Dev Biol 45: 13-38.
95. Spratling MW. 2010. Predictive coding as a model of response properties in cortical area V1. J Neurosci 30: 3531-3543.
96. Stanisor L, van der Togt C, Pennartz CM, Roelfsema PR. 2013. A unified selection signal for attention and reward in primary visual cortex. Proc Natl Acad Sci 110: 9136-9141.
97. Stone JV. 1998. Object recognition using spatiotemporal signatures. Vision Res 38: 947-951.
98. Stone JV. 1999. Object recognition: view-specificity and motion-specificity. Vision Res 39: 4032-4044.
99. Sullivan MJ, Cunningham JT, Mazzella D, Allen AM, Nissen R, Renaud LP. 2003. Lesions of the diagonal band of broca enhance drinking in the rat. J Neuroendocrinol 15: 907-915.
100. Tavazoie S. 2013. Synaptic state matching: a dynamical architecture for predictive internal representation and feature detection. PLoS One 8: e72865.
101. Thomas J, Vanni-Mercier G, Dreher JC. 2013. Neural dynamics of reward probability coding: a Magnetoencephalographic study in humans. Front Neurosci 7: 214.
102. Vogels R. 2010. Mechanisms of visual perceptual learning in macaque visual cortex. Top Cogn Sci 2: 239-250.
103. Vuong QC, Tarr MJ. 2004. Rotation direction affects object recognition. Vision Res 44: 1717-1730.
104. Wacongne C, Changeux JP, Dehaene S. 2012. A neuronal model of predictive coding accounting for the mismatch negativity. J Neurosci 32: 3665-3678.
105. Wagor E, Mangini NJ, Pearlman AL. 1980. Retinotopic organization of striate and extrastriate visual cortex in the mouse. J Comp Neurol 193: 187-202.
106. Wallis G. 2002. The role of object motion in forging long-term representations of objects. Vis Cogn 9: 233-247.
107. Wang X-J. 2013. The prefrontal cortex as a quintessential "cognitive-type" neural circuit. Principles of frontal lobe function, 2nd ed. Oxford University Press, New York.
108. Wang Q, Burkhalter A. 2007. Area map of mouse visual cortex. J Comp Neurol 502: 339-357.
109. Watanabe Y, Funahashi S. 2004. Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. II. Activity encoding visual versus motor signal. J Neurophysiol 92: 1756-1769.
110. Watanabe T, Nanez JE Sr, Koyama S, Mukai I, Liederman J, Sasaki Y. 2002. Greater plasticity in lower-level than higher-level visual motion processing in a passive perceptual learning task. Nat Neurosci 5: 1003-1009.
111. Weinberger NM. 2004. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5: 279-290.
112. Weinberger N. 2011. Reconceptualizing the primary auditory cortex: learning, memory and specific plasticity. In The auditory cortex (ed. Winer JA, Schreiner CE), pp. 465-491. Springer, New York.
113. Wiesel TN, Hubel DH. 1963a. Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26: 978-993.
114. Wiesel TN, Hubel DH. 1963b. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26: 1003-1017.
115. Wiesel TN, Hubel DH. 1965. Extent of recovery from the effects of visual deprivation in kittens. J Neurophysiol 28: 1060-1072.
116. Xu S, Jiang W, Poo MM, Dan Y. 2012. Activity recall in a visual cortical ensemble. Nat Neurosci 15: 449-455, S441-S442.