Olfactory maps, circuits and computations

Current Opinion in Neurobiology

Volumn 24, Issue 1, 2014, Pages 120-132

  Giessel, Andrew J ^a   Datta, Sandeep Robert ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN; LEARNING; MICROCIRCUITRY; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NEUROMODULATION; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY NERVOUS SYSTEM; OLFACTORY NUCLEUS; OLFACTORY RECEPTOR; OLFACTORY STIMULUS; PRIORITY JOURNAL; PYRIFORM CORTEX; REVIEW; SENSORY NERVE; SENSORY STIMULATION;

ANIMALS; BRAIN MAPPING; HUMANS; MODELS, NEUROLOGICAL; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION;

EID: 84886863547     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.09.010     Document Type: Review

References (134)

1. Murthy V.N. Olfactory maps in the brain. Annu Rev Neurosci 2011, 34:233-258.
2. Petersen C.C. The functional organization of the barrel cortex. Neuron 2007, 56:339-355.
3. Luo L., Flanagan J.G. Development of continuous and discrete neural maps. Neuron 2007, 56:284-300.
4. Layton O.W., Mingolla E., Yazdanbakhsh A. Dynamic coding of border-ownership in visual cortex. J Vis 2012, 12:8.
5. Gonzalez F., Perez R. Neural mechanisms underlying stereoscopic vision. Prog Neurobiol 1998, 55:191-224.
6. Clifford C.W., Ibbotson M.R. Fundamental mechanisms of visual motion detection: models, cells and functions. Prog Neurobiol 2002, 68:409-437.
7. Amoore J.E. Stereochemical and vibrational theories of odour. Nature 1971, 233:270-271.
8. Bathellier B., Buhl D.L., Accolla R., Carleton A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 2008, 57:586-598.
9. Friedrich R.W., Stopfer M. Recent dynamics in olfactory population coding. Curr Opin Neurobiol 2001, 11:468-474.
10. Gire D.H., Restrepo D., Sejnowski T.J., Greer C., De Carlos J.A., Lopez-Mascaraque L. Temporal processing in the olfactory system: can we see a smell?. Neuron 2013, 78:416-432.
11. Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 2002, 3:884-895.
12. Mandairon N., Linster C. Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 2009, 101:2204-2209.
13. Wilson D.A., Sullivan R.M., Leon M. Single-unit analysis of postnatal olfactory learning: modified olfactory bulb output response patterns to learned attractive odors. J Neurosci 1987, 7:3154-3162.
14. Wilson R.I., Mainen Z.F. Early events in olfactory processing. Annu Rev Neurosci 2006, 29:163-201.
15. Kandel E.R. Principles of Neural Science 2013, McGraw-Hill Medical, New York. 5th edn.
16. Sheperd G.M., Chen W.R., Greer C.A. Olfactory Bulb 2004, Oxford University Press, Oxford, NY. 5th edn. G.M. Shepherd (Ed.).
17. Ramón, Cajal S. Histologie du systeme nerveux de l'homme et des vertebres 1911, Maloine, Paris.
18. Axel R. The molecular logic of smell. Sci Am 1995, 273:154-159.
19. Mori K., Shepherd G.M. Emerging principles of molecular signal processing by mitral/tufted cells in the olfactory bulb. Seminars Cell Biol 1994, 5:65-74.
20. Wachowiak M., Shipley M.T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Seminars Cell Develop Biol 2006, 17:411-423.
21. Wellis D.P., Scott J.W., Harrison T.A. Discrimination among odorants by single neurons of the rat olfactory bulb. J Neurophysiol 1989, 61:1161-1177.
22. Neville KRaH L.B. Olfactory Cortex 2004, Oxford University Press, Oxford, NY. 5th edn. G.M. Shepherd (Ed.).
23. Allison A.C. The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. J Comp Neurol 1953, 98:309-353.
24. Broadwell R.D. Olfactory relationships of the telencephalon and diencephalon in the rabbit. I. An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs. J Comp Neurol 1975, 163:329-345.
25. Haberly L.B., Price J.L. The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 1977, 129:152-157.
26. Heimer L. Synaptic distribution of centripetal and centrifugal nerve fibres in the olfactory system of the rat. An experimental anatomical study. J Anat 1968, 103:413-432.
27. Land L.J., Eager R.P., Shepherd G.M. Olfactory nerve projections to the olfactory bulb in rabbit: demonstration by means of a simplified ammoniacal silver degeneration method. Brain Res 1970, 23:250-254.
28. Price J.L. An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 1973, 150:87-108.
29. Scalia F., Halpern M., Knapp H., Riss W. The efferent connexions of the olfactory bulb in the frog: a study of degenerating unmyelinated fibres. J Anat 1968, 103:245-262.
30. Scott J.W., McBride R.L., Schneider S.P. The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J Comparative Neurol 1980, 194:519-534.
31. White L.E. Olfactory bulb projections of the rat. Anat Record 1965, 152:465-479.
32. Buonviso N., Revial M.F., Jourdan F. The projections of mitral cells from small local regions of the olfactory bulb: an anterograde tracing study using PHA-L (Phaseolus vulgaris Leucoagglutinin). Eur J Neurosci 1991, 3:493-500.
33. Ojima H., Mori K., Kishi K. The trajectory of mitral cell axons in the rabbit olfactory cortex revealed by intracellular HRP injection. J Comparative Neurol 1984, 230:77-87.
34. Davis B.J., Macrides F., Youngs W.M., Schneider S.P., Rosene D.L. Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Res Bull 1978, 3:59-72.
35. Yan Z., Tan J., Qin C., Lu Y., Ding C., Luo M. Precise circuitry links bilaterally symmetric olfactory maps. Neuron 2008, 58:613-624.
36. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell 1996, 87:675-686.
37. Ressler K.J., Sullivan S.L., Buck L.B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 1993, 73:597-609.
38. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell 1994, 79:981-991.
39. Sosulski D.L., Bloom M.L., Cutforth T., Axel R., Datta S.R. Distinct representations of olfactory information in different cortical centres. Nature 2011, 472:213-216.
40. Ghosh S., Larson S.D., Hefzi H., Marnoy Z., Cutforth T., Dokka K., Baldwin K.K. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 2011, 472:217-220.
41. Miyamichi K., Amat F., Moussavi F., Wang C., Wickersham I., Wall N.R., Taniguchi H., Tasic B., Huang Z.J., He Z., et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 2011, 472:191-196.
42. Haberly L.B., Bower J.M. Olfactory cortex: model circuit for study of associative memory?. Trends Neurosci 1989, 12:258-264.
43. Isaacson J.S. Odor representations in mammalian cortical circuits. Curr Opin Neurobiol 2010, 20:328-331.
44. Wilson D.A., Kadohisa M., Fletcher M.L. Cortical contributions to olfaction: plasticity and perception. Seminars Cell Develop Biol 2006, 17:462-470.
45. Wilson D.A., Sullivan R.M. Cortical processing of odor objects. Neuron 2011, 72:506-519.
46. Stokes C.C.A., Isaacson J.S. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 2010, 67:452-465.
47. Suzuki N., Bekkers J.M. Inhibitory interneurons in the piriform cortex - Suzuki - 2007 - clinical and experimental pharmacology and physiology - Wiley Online Library. Clin Exp Pharmacol Physiol 2007, 34:1064-1069.
48. Suzuki N., Bekkers J.M. Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex. Cereb Cortex 2010, 20:2971-2984.
49. Suzuki N., Bekkers J.M. Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comparative Neurol 2010, 518:1670-1687.
50. Suzuki N., Bekkers J.M. Microcircuits mediating feedforward and feedback synaptic inhibition in the piriform cortex. J Neurosci 2012, 32:919-931.
51. Poo C., Isaacson J.S. Odor representations in olfactory cortex: 'sparse' coding, global inhibition, and oscillations. Neuron 2009, 62:850-861.
52. Poo C., Isaacson J.S. A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 2011, 72:41-48.
53. Suzuki N., Bekkers J.M. Two layers of synaptic processing by principal neurons in piriform cortex. J Neurosci 2011, 31:2156-2166.
54. Hagiwara A., Pal S.K., Sato T.F., Wienisch M., Murthy V.N. Optophysiological analysis of associational circuits in the olfactory cortex. Front Neural Circuits 2012, 6:18.
55. Bekkers J.M., Suzuki N. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci 2013, 36:429-438.
56. Franks K.M., Isaacson J.S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 2006, 49:357-363.
57. Franks K.M., Russo M.J., Sosulski D.L., Mulligan A.A., Siegelbaum S.A., Axel R. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 2011, 72:49-56.
58. Davison I.G., Ehlers M.D. Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 2011, 70:82-94.
59. Haddad R., Lanjuin A., Madisen L., Zeng H., Murthy V.N., Uchida N. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat Neurosci 2013, 16:949-957.
60. Fukunaga I., Berning M., Kollo M., Schmaltz A., Schaefer A.T. Two distinct channels of olfactory bulb output. Neuron 2012, 75:320-329.
61. Gire D.H., Whitesell J.D., Doucette W., Restrepo D. Information for decision-making and stimulus identification is multiplexed in sensory cortex. Nat Neurosci 2013, 16:991-993.
62. Zhan C., Luo M. Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice. J Neurosci 2010, 30:16662-16672.
63. Gale K. Subcortical structures and pathways involved in convulsive seizure generation. J Clin Neurophysiol 1992, 9:264-277.
64. Löscher W., Ebert U. The role of the piriform cortex in kindling. Progr Neurobiol 1996, 50:427-481.
65. Barnes D.C., Hofacer R.D., Zaman A.R., Rennaker R.L., Wilson D.A. Olfactory perceptual stability and discrimination. Nat Neurosci 2008, 11:1378-1380.
66. Kadohisa M., Wilson D.A. Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 2006, 95:1888-1896.
67. Kadohisa M., Wilson D.A. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci USA 2006, 103:15206-15211.
68. Litaudon P., Amat C., Bertrand B., Vigouroux M., Buonviso N. Piriform cortex functional heterogeneity revealed by cellular responses to odours. Eur J Neurosci 2003, 17:2457-2461.
69. Miura K., Mainen Z.F., Uchida N. Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 2012, 74:1087-1098.
70. Payton C.A., Wilson D.A., Wesson D.W. Parallel odor processing by two anatomically distinct olfactory bulb target structures. PLoS One 2012, 7:e34926.
71. Rennaker R.L., Chen C-F.F., Ruyle A.M., Sloan A.M., Wilson D.A. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J Neurosci 2007, 27:1534-1542.
72. Stettler D.D., Axel R. Representations of odor in the piriform cortex. Neuron 2009, 63:854-864.
73. Wilson D.A. Habituation of odor responses in the rat anterior piriform cortex. J Neurophysiol 1998, 79:1425-1440.
74. Wilson D.A. Odor specificity of habituation in the rat anterior piriform cortex. J Neurophysiol 2000, 83:139-145.
75. Wilson D.A. Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J Neurophysiol 2003, 90:65-72.
76. Illig K.R., Haberly L.B. Odor-evoked activity is spatially distributed in piriform cortex. J Comparative Neurol 2003, 457:361-373.
77. Linster C., Wyble B.P., Hasselmo M.E. Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. J Neurophysiol 1999, 81:2737-2742.
78. Luskin M.B., Price J.L. The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling techniques. J Comparative Neurol 1982, 209:249-263.
79. Barkai E., Bergman R.E., Horwitz G., Hasselmo M.E. Modulation of associative memory function in a biophysical simulation of rat piriform cortex. J Neurophysiol 1994, 72:659-677.
80. Hasselmo M.E., Bower J.M. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 1992, 67:1222-1229.
81. Patil M.M., Hasselmo M.E. Modulation of inhibitory synaptic potentials in the piriform cortex. J Neurophysiol 1999, 81:2103-2118.
82. Patil M.M., Linster C., Lubenov E., Hasselmo M.E. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol 1998, 80:2467-2474.
83. Linster C., Hasselmo M.E. Neuromodulation and the functional dynamics of piriform cortex. Chem Senses 2001, 26:585-594.
84. Hasselmo M.E., Sarter M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 2011, 36:52-73.
85. Hasselmo M.E., McGaughy J. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Progr Brain Res 2004, 145:207-231.
86. Chapuis J., Wilson D.A. Cholinergic modulation of olfactory pattern separation. Neurosci Lett 2013, 545:50-53.
87. Hasselmo M.E., Anderson B.P., Bower J.M. Cholinergic modulation of cortical associative memory function. J Neurophysiol 1992, 67:1230-1246.
88. Millhouse O.E., Heimer L. Cell configurations in the olfactory tubercle of the rat. J Comparative Neurol 1984, 228:571-597.
89. Wesson D.W., Wilson D.A. Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics, sensory integration, and more?. Neurosci Biobehav Rev 2011, 35:655-668.
90. Heimer L., Wilson R.D. The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. Golgi Centennial Symposium Proceedings 1975.
91. Heimer L., Zaborszky L., Zahm D.S., Alheid G.F. The ventral striatopallidothalamic projection: I. The striatopallidal link originating in the striatal parts of the olfactory tubercle. J Comparative Neurol 1987, 255:571-591.
92. Zahm D.S., Heimer L. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comparative Neurol 1993, 327:220-232.
93. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 2007, 56:27-78.
94. Luskin M.B., Price J.L. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comparative Neurol 1983, 216:264-291.
95. Bertran-Gonzalez J., Bosch C., Maroteaux M., Matamales M., Hervé D., Valjent E., Girault J-A. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 2008, 28:5671-5685.
96. Le Moine C., Bloch B. D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAS in distinct neuronal populations of the dorsal and ventral striatum. J Comparative Neurol 1995, 355:418-426.
97. Fallon J.H. The islands of Calleja complex of rat basal forebrain II: connections of medium and large sized cells. Brain Res Bull 1983, 10:775-793.
98. Fallon J.H., Loughlin S.E., Ribak C.E. The islands of Calleja complex of rat basal forebrain. III. Histochemical evidence for a striatopallidal system. J Comparative Neurol 1983, 218:91-120.
99. Fallon J.H., Riley J.N., Sipe J.C., Moore R.Y. The islands of Calleja: organization and connections. J Comparative Neurol 1978, 181:375-395.
100. Adjei S., Houck A.L., Ma K., Wesson D.W. Age-dependent alterations in the number, volume, and localization of islands of Calleja within the olfactory tubercle. Neurobiol Aging 2013, 34:2676-2682.
101. Hsieh Y-C., Puche A.C. Development of the Islands of Calleja. Brain Res 2013, 1490:52-60.
102. McNamara A.M. Characterization of the synaptic properties of olfactory bulb projections. Chem Senses 2004, 29:225-233.
103. Owen G.S., Halliwell J.V. Electrophysiological characterization of laminar synaptic inputs to the olfactory tubercle of the rat studied in vitro: modulation of glutamatergic transmission by cholinergic agents is pathway-specific. Eur J Neurosci 2001, 13:1767-1780.
104. Carriero G., Uva L., Gnatkovsky V., de Curtis M. Distribution of the olfactory fiber input into the olfactory tubercle of the in vitro isolated guinea pig brain. J Neurophysiol 2009, 101:1613-1619.
105. Chiang E., Strowbridge B.W. Diversity of neural signals mediated by multiple, burst-firing mechanisms in rat olfactory tubercle neurons. J Neurophysiol 2007, 98:2716-2728.
106. Halliwell J.V., Horne A.L. Evidence for enhancement of gap junctional coupling between rat island of Calleja granule cells in vitro by the activation of dopamine D3 receptors. J Physiol 1998, 506(Pt 1):175-194.
107. Rampin O., Bellier C., Maurin Y. Electrophysiological responses of rat olfactory tubercle neurons to biologically relevant odours. Eur J Neurosci 2011, 35:97-105.
108. Wesson D.W., Wilson D.A. Smelling sounds: olfactory-auditory sensory convergence in the olfactory tubercle. J Neurosci 2010, 30:3013-3021.
109. Hagamen T.C., Greeley H.P., Hagamen W.D., Reeves A.G. Behavioral asymmetries following olfactory tubercle lesions in cats. Brain Behav Evol 1977, 14:241-250.
110. Ikemoto S. Involvement of the olfactory tubercle in cocaine reward: intracranial self-administration studies. J Neurosci 2003, 23:9305-9311.
111. Koob G.F., Riley S.J., Smith S.C., Robbins T.W. Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. J Comparative Physiol Psychol 1978, 92:917-927.
112. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 2011, 34:441-466.
113. Kreitzer A.C. Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 2009, 32:127-147.
114. Lerner T.N., Kreitzer A.C. Neuromodulatory control of striatal plasticity and behavior. Curr Opin Neurobiol 2011, 21:322-327.
115. Nicola S.M., Hopf F.W., Hjelmstad G.O. Contrast enhancement: a physiological effect of striatal dopamine?. Cell Tissue Res 2004, 318:93-106.
116. Wilson D.A., Stevenson R.J. Olfactory perceptual learning: the critical role of memory in odor discrimination. Neurosci Biobehav Rev 2003, 27:307-328.
117. Choi G.B., Stettler D.D., Kallman B.R., Bhaskar S.T., Fleischmann A., Axel R. Driving opposing behaviors with ensembles of piriform neurons. Cell 2011, 146:1004-1015.
118. Cohen M.X., Frank M.J. Neurocomputational models of basal ganglia function in learning, memory and choice. Behav Brain Res 2009, 199:141-156.
119. Pennartz C.M., Groenewegen H.J., Lopes da Silva F.H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Progr Neurobiol 1994, 42:719-761.
120. Schultz W. Potential vulnerabilities of neuronal reward, risk, and decision mechanisms to addictive drugs. Neuron 2011, 69:603-617.
121. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nat Rev Neurosci 2006, 7:464-476.
122. Ponzi A., Wickens J. Cell assemblies in large sparse inhibitory networks of biologically realistic spiking neurons. 21st conference of Advances in Neural Information Processing Systems, vol. 2 2008, 1276-1283. http://www.proceedings.com/05012.html.
123. Ponzi A., Wickens J. Sequentially switching cell assemblies in random inhibitory networks of spiking neurons in the striatum. J Neurosci 2010, 30:5894-5911.
124. Ponzi A., Wickens J. Input dependent cell assembly dynamics in a model of the striatal medium spiny neuron network. Front Systems Neurosci 2012, 6:6.
125. Taverna S., Ilijic E., Surmeier D.J. Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J Neurosci 2008, 28:5504-5512.
126. Tepper J.M., Koós T., Wilson C.J. GABAergic microcircuits in the neostriatum. Trends Neurosci 2004, 27:662-669.
127. Tunstall M.J., Oorschot D.E., Kean A., Wickens J.R. Inhibitory interactions between spiny projection neurons in the rat striatum. J Neurophysiol 2002, 88:1263-1269.
128. Reynolds S.M., Berridge K.C. Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci 2008, 11:423-425.
129. Roitman M.F., Wheeler R.A., Carelli R.M. Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 2005, 45:587-597.
130. Setlow B., Schoenbaum G., Gallagher M. Neural encoding in ventral striatum during olfactory discrimination learning. Neuron 2003, 38:625-636.
131. Cui G., Jun S.B., Jin X., Pham M.D., Vogel S.S., Lovinger D.M., Costa R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 2013, 494:238-242.
132. Jin X., Costa R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 2010, 466:457-462.
133. Yin H.H., Mulcare S.P., Hilário M.R.F., Clouse E., Holloway T., Davis M.I., Hansson A.C., Lovinger D.M., Costa R.M. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 2009, 12:333-341.
134. Kobayakawa K., Kobayakawa R., Matsumoto H., Oka Y., Imai T., Ikawa M., Okabe M., Ikeda T., Itohara S., Kikusui T., et al. Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450:503-508.