Olfactory perceptual learning: The critical role of memory in odor discrimination

Neuroscience and Biobehavioral Reviews

Volumn 27, Issue 4, 2003, Pages 307-328

  Wilson, Donald A ^a   Stevenson, Richard J ^b  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

Odor discrimination; Olfactory bulb; Olfactory coding; Olfactory memory; Olfactory psychophysics; Perceptual learning; Piriform cortex; Synthetic coding

Indexed keywords

SCOPOLAMINE;

ASSOCIATIVE MEMORY; BEHAVIORAL SCIENCE; CONDITIONING; CONSCIOUSNESS; EVOKED CORTICAL RESPONSE; EXTRACTION; FEAR; HABITUATION; HUMAN; LEARNING; LEARNING TEST; MAZE TEST; NERVE CELL PLASTICITY; NEUROBIOLOGY; NEUROPHYSIOLOGY; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY DISCRIMINATION; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; PSYCHOBIOLOGY; PSYCHOPHYSICS; PYRIFORM CORTEX; REVIEW; SMELLING;

EID: 0041734613     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(03)00050-2     Document Type: Review

References (189)

1. Adrian E.D. The electrical activity of the olfactory bulb. EEG Clin Neurophysiol. 2:1950;377-388.
2. Amoore J.E. Specific anosmia: a clue to the olfactory code. Nature. 214:1967;1095-1098.
3. Amoore J.E. Molecular basis of odor. 1970;Charles C. Thomas, Springfield, IL.
4. Annett J.M., Leslie J.C. Effects of visual and verbal interference on olfactory memory: the role of task complexity. Br J Psychol. 87:1996;447-457.
5. Araneda R.C., Kini A.D., Firestein S. The molecular receptive range of an odorant receptor. Nat Neurosci. 3:2000;1248-1255.
6. Ayabe-Kanamura S., Schicker I., Laska M., Hudson R., Distel H., Kobayakawa T., Saito S. Differences in perception of everyday odors: a Japanese-German cross cultural study. Chem Senses. 23:1998;31-38.
7. 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. 72:1994;659-677.
8. Bazhenov M., Stopfer M., Rabinovich M., Abarbanel H.D.I., Sejnowski T.J., Laurent G. Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron. 30:2001;569-581.
9. Belluscio L., Lodovichi C., Feinstein P., Mombaerts P., Katz L.C. Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature. 419:2002;296-300.
10. Bende M., Nordin S. Perceptual learning in olfaction: professional wine tasters versus controls. Physiol Behav. 62:1997;1065-1070.
11. Best AR, Wilson DA. Synaptic correlates of cortical adaptation. Society for Neurosciences Abstracts; 2002.
12. Bouret S., Sara S.J. Locus coeruleus activation modulates firing rate and temporal organization of odour-induced single-cell responses in rat piriform cortex. Eur J Neurosci. 16:2002;2371-2382.
13. Bozza T.C., Kauer J.S. Odorant response properties of convergent olfactory receptor neurons. J Neurosci. 18:1998;4560-4569.
14. Brennan P.A., Keverne E.B. Neural mechanisms of mammalian olfactory learning. Prog Neurobiol. 51:1997;457-481.
15. Bressler S.L. Changes in electrical activity of rabbit olfactory bulb and cortex to conditioned odor stimulation. Behav Neurosci. 102:1988;740-747.
16. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular bases for odor recognition. Cell. 65:1991;175-187.
17. Bult J.H.F., Schifferstein H.N.J., Roozen J.P., Voragen A.G.J., Kroeze J.H.A. The influence of olfactory concept on the probability of detecting sub- and peri-threshold components in a mixture of odorants. Chem Senses. 26:2001;459-469.
18. 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 Leuco-agglutinin). Eur J Neurosci. 3:1991;493-500.
19. Cain W.S., Schmidt R. Sensory detection of glutaraldehyde in drinking water - emergense of sensitivity and specific anosmia. Chem Senses. 27:2002;425-433.
20. Case TI, Stevenson RJ, Boakes RA. Olfactory perceptual learning: acquired equivalence and acquired distinctiveness. Submitted.
21. Cattarelli M., Astic L., Kauer J.S. Metabolic mapping of 2DG uptake in the rat piriform cortex using computerized image processing. Brain Res. 442:1988;180-184.
22. Chabaud P., Ravel N., Wilson D.A., Mouly A.M., Vigouroux M., Farget V., Gervais R. Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem Senses. 25:2000;561-573.
23. Christensen T.A., Pawlowski V.M., Lei H., Hildebrand J.G. Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat Neurosci. 3:2000;927-931.
24. Dalton P., Doolittle N., Nagata H., Breslin P.A.S. The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci. 3:2000;431-432.
25. Derby C.D., Ache B.W. Quality coding of a complex odorant in an invertebrate. J Neurophysiol. 51:1984;906-924.
26. DeRosa E., Hasselmo M.E. Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci. 114:2000;32-41.
27. Dittman A.H., Quinn T.P., Nevitt G.A., Hacker B., Storm D.R. Sensitization of olfactory guanylyl cyclase to a specific imprinted odorant in Coho salmon. Neuron. 19:1997;381-389.
28. Duchamp-Viret P., Palouzier-Paulignan B., Duchamp A. Odor coding properties of frog olfactory cortical neurons. Neuroscience. 74:1996;885-895.
29. Eeckman F.H., Freeman W.J. Correlations between unit firing and EEG in the rat olfactory system. Brain Res. 528:1990;238-244.
30. Eichenbaum H., Morton T.H., Potter H., Corkin S. Selective olfactory deficits in case H.M. Brain. 106:1983;459-472.
31. Eichenbaum H. Using olfaction to study memory. Ann N Y Acad Sci. 855:1998;657-669.
32. Engen T. Odor sensation and memory. 1991;Praeger, New York.
33. Engen T., Lipsitt L.P. Decrement and recovery of responses to olfactory stimuli in the human neonate. J Comp Physiol Psychol. 59:1965;312-316.
34. Fahle M. Figure-ground discrimination from temporal information. Proc R Soc Lond B. 254:1993;199-203.
35. Firestein S. How the olfactory system makes sense of scents. Nature. 413:2001;211-218.
36. Fletcher M.L., Wilson D.A. Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats. Physiol Behav. 74:2001;589-593.
37. Fletcher M.L., Wilson D.A. Experience modifies olfactory acuity: acetylcholine-dependent learning decreases behavioral generalization between similar odorants. J Neurosci. 22:2002;RC201(1-5).
38. Fox A.N., Pitts R.J., Robertson H.M., Carlson J.R., Zwiebel L.J. Candidate odorant receptors from malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc Natl Acad Sci USA. 98:2001;14693-14697.
39. Frank R.A., Byram J. Taste-smell interactions are tastant and odorant dependent. Chem Sens. 13:1988;445-455.
40. Freeman W.J. Spatial properties of an EEG event in the olfactory bulb and cortex. EEG Clin Neurophysiol. 44:1978;586-605.
41. Freeman W.J. Neurodynamics: an exploration in mesoscopic brain dynamics. 2000;Springer, New York.
42. Friedrich R.W., Korsching S.I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron. 18:1997;737-752.
43. Friedrich R.W., Stopfer M. Recent dynamics in olfactory population coding. Curr Opin Neurobiol. 11:2001;468-474.
44. Gaillard I., Rouquier S., Pin J.P., Mollard P., Richard S., Barnabe C., Demaille J., Giorgi D. A single olfactory receptor specifically binds a set of odorant molecules. Eur J Neurosci. 15:2002;409-418.
45. Gesteland R.C., Lettvin J.Y., Pitts W.H. Chemical transmission in the nose of the frog. J Physiol. 181:1965;525-559.
46. Ghazanfar A.A., Krupa D.J., Nicolelis M.A.L. Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons. Exp Brain Res. 141:2001;88-100.
47. Gilbert C.D., Sigman M., Crist R.E. The neural basis of perceptual learning. Neuron. 31:2001;681-697.
48. Girardot M.N., Derby C.D. Neural coding of quality of complex olfactory stimuli in lobsters. J Neurophysiol. 60:1988;303-324.
49. Giraudet P., Berthommier F., Chaput M. Mitral cell temporal response patterns evoked by odor mixtures in the rat olfactory bulb. J Neurophysiol. 88:2002;829-838.
50. Granger R., Lynch G. Higher olfactory processes: Perceptual learning and memory. Curr Opin Neurobiol. 1:1991;209-214.
51. Guthrie K.M., Gall C. Anatomic mapping of neuronal odor responses in the developing rat olfactory bulb. J Comp Neurol. 455:2003;56-71.
52. Haberly L.B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses. 26:2001;551-576.
53. Hasselmo M.E., Barkai E. Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci. 15:1995;6592-6604.
54. Hasselmo M.E., Linster C., Patil M., Ma D., Cekic M. Noradrenergic suppression of synaptic transmission may influence cortical signal-to-noise ratio. J Neurophysiol. 77:1997;3326-3339.
55. Hudson R. Olfactory imprinting. Curr Opin Neurobiol. 3:1993;548-552.
56. Hudson R. From molecule to mind: the role of experience in shaping olfactory function. J Comp Physiol. 185A:1999;297-304.
57. Illig K.R., Haberly L.B. Odor-evoked activity is spatially distributed in piriform cortex. J Comp Neurol. 457:2003;361-373.
58. Jehl C., Royet J.P., Holley A. Odor discrimination and recognition memory as a function of familiarization. Percept Psychophys. 57:1995;1002-1011.
59. Jellinek J.S., Koster E.P. Perceived fragrance complexity and its relation to familiarity and pleasantness. J Soc Cosmet Chem. 30:1979;253-262.
60. Jinks A., Laing D.G. A limit in the processing of components in odour mixtures. Percept. 28:1999;395-404.
61. Jinks A., Laing D.G. The analysis of odor mixtures by humans: evidence for a configurational process. Physiol Behav. 72:2002;51-63.
62. Joerges J, Kuttner A, Galizia CG, Menzel R. Representations of odours and odour mixtures visualized in the honeybee brain. Nature 1997:285-8.
63. Johnson B.A., Woo C.C., Leon M. Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J Comp Neurol. 393:1998;457-471.
64. Johnson B.A., Leon M. Odorant molecular length: one aspect of the olfactory code. J Comp Neurol. 426:2000;330-338.
65. Jourdan F., Duveau L., Astic L., Holley A. Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours. Brain Res. 188:1980;139-154.
66. Jung M.W., Larson J., Lynch G. Long-term potentiation of monosynaptic EPSPs in rat piriform cortex in vitro. Synapse. 6:1990;279-283.
67. Kaluza J.F., Breer H. Responsiveness of olfactory neurons to distinct aliphatic aldehydes. J Exp Biol. 203:2000;927-933.
68. Kanter E.D., Haberly L.B. NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro. Brain Res. 525:1990;175-179.
69. Kashiwadani H., Sasaki Y.F., Uchida N., Mori K. Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J Neurophysiol. 82:1999;1786-1792.
70. Katoh K., Koshimoto H., Tani A., Mori K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. J Neurophysiol. 70:1993;2161-2175.
71. Kent P.F., Mozell M.M. The recording of odorant-induced mucosal activity patterns with a voltage-sensitive dye. J Neurophysiol. 68:1992;1804-1819.
72. Laing D.G., Francis G.W. The capacity of humans to identify odors in mixtures. Physiol Behav. 46:1989;809-814.
73. Laing D.G., Glenmarec A. Selective attention and the perceptual analysis of odor mixtures. Physiol Behav. 52:1992;1047-1053.
74. Laing D.G., Legha P.K., Jinks A.L., Hutchinson I. Relationship between molecular structure, concentration and odor qualities of oxygenated aliphatic molecules. Chem Senses. 28:2003;57-69.
75. Laurent G.J., Bazhenov M., Stopfer M., Sejnowski T.J. Fast odor learning and reliability of odor responses in the locust antennal lobe. Soc Neurosci Abstracts. 2002.
76. Laurent G., Stopfer M., Friedrich R.W., Rabinovich M.I., Volkovskii A., Abarbanel H.D.I. Odor encoding as an active, dynamical process: experiments, computation, and theory. Ann Rev Neurosci. 24:2001;263-297.
77. Lei H., Christensen T.A., Hildebrand J.G. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci. 5:2002;557-565.
78. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature. 405:2000;792-796.
79. Li L., Miller E.K., Desimone R. The representation of stimulus familiarity in anterior inferior temporal cortex. J Neurophysiol. 69:1993;1918-1929.
80. Linster C., Johnson B.A., Morse A., Yue E., Leon M. Spontaneous versus reinforced olfactory discriminations. J Neurosci. 22:2002;6842-6845.
81. Linster C., Smith B.H. Generalization between binary odor mixtures and their components in the rat. Physiol Behav. 66:1999;701-707.
82. Litaudon P., Mouly A.M., Sullivan R., Gervais R., Cattarelli M. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur J Neurosci. 9:1997;1593-1602.
83. Livermore A., Laing D.G. Influence of training and experience on the perception of multicomponent odor mixtures. J Exp Psychol Hum Percept Perform. 22:1996;267-277.
84. Livermore A., Laing D.G. The influence of chemical complexity on the perception of multicomponent odor mixtures. Percept Psychophys. 60:1998;650-661.
85. Livermore A., Laing D.G. The influence of odor type on the discrimination and identification of odorants in multicomponent odor mixtures. Physiol Behav. 65:1998;311-320.
86. Lowe G., Gold G.H. The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J Physiol. 442:1991;147-168.
87. Lu X.C.M., Slotnick B.M. Olfaction in rats with extensive lesions of the olfactory bulb: implications for odor coding. Neuroscience. 84:1998;849-866.
88. Luo M., Katz L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron. 32:2001;1165-1179.
89. Mackay-Sim A., Kesteven S. Topographic patterns of responsiveness to odorants in the rat olfactory epithelium. J Neurophysiol. 71:1994;150-160 Mair R.G., Gesteland R.C. Response properties of mitral cells in the olfactory bulb of the neonatal rat. Neuroscience. 7:1982;3117-3125.
90. Mackay-Sim A., Kesteven S. Topographic patterns of responsiveness to odorants in the rat olfactory epithelium. J Neurophysiol. 71:1994;150-160 Mair R.G., Gesteland R.C. Response properties of mitral cells in the olfactory bulb of the neonatal rat. Neuroscience. 7:1982;3117-3125.
91. Mair R., Harrison L.M., Flint D.L. The neuropsychology of odor memory. Schab F.R., Crowder R.G. Memory for odors. 1995;39 LEA, New Jersey.
92. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell. 96:1999;713-723.
93. McCollum J., Larson J., Otto T., Schottler F., Granger R., Lynch G. Short-latency single-unit processing in olfactory cortex. J Cogn Neurosci. 3:1991;293-299.
94. Melcher J.M., Schooler J.W. The misrememberance of wines past: verbal and perceptual expertise differentially mediate verbal overshadowing of taste memory. J Mem Lang. 35:1996;231-245.
95. Mennella J.A., Beauchamp G.K. Infants exploration of scented toys; effects of prior experiences. Chem Senses. 23:1998;11-17.
96. Miyashita Y., Hayashi T. Neural representation of visual objects: encoding and top-down activation. Curr Opin Neurobiol. 10:2000;187-194.
97. Moncrieff R.W. The chemical senses. 1951;Hill, London.
98. Mori K., Nagao H., Yoshihara Y. The olfactory bulb: coding and processing of odor molecule information. Science. 286:1999;711-715.
99. Moskowitz H.R., Barbe C.D. Profiling of odor components and their mixtures. Sen Proc. 1:1977;212-226.
100. Murphy P.C., Duckett S.G., Sillito A.M. Feedback connections to the lateral geniculate nucleus and cortical response properties. Science. 286:1999;1552-1554.
101. Myles-Worsley M., Johnston W.A., Simons M.A. The influence of expertise on X-ray image processing. J Exp Psychol Learn Mem Cog. 14:1988;553-557.
102. Nagao H., Yamaguchi M., Takahash Y., Mori K. Grouping and representation of odorant receptors in domains of the olfactory bulb sensory map. Microscopy Res Tech. 58:2002;168-175.
103. Najbauer J., Leon M. Olfactory experience modulates apoptosis in the developing olfactory bulb. Brain Res. 674:1995;245-251.
104. Nevitt G.A., Dittman A.H., Quinn T.P., Moody J.W.J. Evidence for a peripheral olfactory memory in imprinted salmon. Proc Natl Acad Sci USA. 91:1994;4288-4292.
105. Nusser Z., Kay L.M., Laurent G., Homanics G.E., Mody I. Disruption to GABA-A receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol. 86:2001;2823-2833.
106. Owen D.H., Machamer P.K. Bias-free improvement in wine discrimination. Percept. 8:1979;199-209.
107. Perez-Orive J., Mazor O., Turner G.C., Cassenaer S., Wilson R.I., Laurent G. Oscillations and sparsening of odor representations in the mushroom body. Science. 297:2002;359-365.
108. Peron R.M., Allen G.L. Attempts to train novices for beer flavor discrimination: a matter of taste. J Gen Psychol. 115:1989;403-418.
109. Petreanu L., Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 22:2002;6106-6113.
110. Pierce J., Halpern B. Orthonasal and retronasal odorant identification based upon vapor phase input from common substances. Chem Sens. 21:1996;529-543.
111. Pierce J.D. Jr., Zeng X.N., Aronov E.V., Preti G., Wysocki C.J. Cross-adaptation of sweaty-smelling 3-methyl-2-hexenoic acid by a structurally-similar, pleasant-smelling odorant. Chem Senses. 20:1995;401-411.
112. Prescott J. Flavour as a psychological construct: implications for perceiving and measuring the sensory qualities of foods. Food Qual Pref. 10:1999;1-8.
113. Rabin M.D. Experience facilitates olfactory quality discrimination. Percept Psychophys. 44:1988;532-540.
114. Rall W., Shepherd G.M. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in the olfactory bulb. J Neurophysiol. 31:1968;884-915.
115. Ravel N., Elaagouby A., Gervais R. Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. Behav Neurosci. 108:1994;317-324.
116. Ressler K.J., Sullivan S.L., Buck L.B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 73:1993;597-609.
117. Ressler K.J., Sullivan S.L., Buck L.B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 79:1994;1245-1255.
118. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci. 22:2002;2679-2689.
119. Rolls E.T., Baylis L.L. Gustatory, olfactory and visual convergence within the primate orbitofrontal cortex. J Neurosci. 14:1994;5437-5452.
120. Rolls E.T. Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition. Neuron. 27:2000;205-218.
121. Roman F.S., Simonetto I., Soumireu-Mourat B. Learning and memory of odor-reward association: selective impairment following horizontal diagonal band lesions. Behav Neurosci. 107:1993;72-81.
122. Roman F., Staubli U., Lynch G. Evidence for synaptic potentiation in a cortical network during learning. Brain Res. 418:1987;221-226.
123. Rozin P. The use of characteristic flavourings in human culinary practice. Apt M. Flavour: its chemical behavioural and commercial aspects. 1978;101-127 Westview Press, Colorado.
124. Rovee C.K. Olfactory cross-adaptation and facilitation in human neonates. J Exp Child Psychol. 13:1972;368-381.
125. Rubin B.D., Katz L.C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron. 23:1999;499-511.
126. Saar D., Grossman F., Barkai E. Long-lasting cholinergic modulation underlies rule learning in rats. J Neurosci. 21:2001;1385-1392.
127. Saar D., Grossman Y., Barkai E. Learning-induced enhancement of postsynaptic potentials in pyramidal neurons. J Neurophysiol. 87:2002;2358-2363.
128. Sakai N., Imada S. Bilateral lesion of the insular cortex or of the prefrontal cortex block the association between taste and odor in the rat. Neurobiol Learn Mem. 80:2003;24-31.
129. Sakai N., Yamamoto T. Effects of excitotoxic lesions on taste-mediated odor learning in the rat. Neurobiol Learn Mem. 75:2001;128-139.
130. Sato T., Hirono J., Tonoike M., Takebayashi M. Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. J Neurophysiol. 72:1994;2980-2989.
131. Schoenbaum G., Eichenbaum H. Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J Neurophysiol. 74:1995;733-750.
132. Scott J.W., Brierley T., Schmidt F.H. Chemical determinants of the rat electro-olfactogram. J Neurosci. 20:2000;4721-4731.
133. Sekiguchi T., Suzuki H., Yamada A., Kimura T. Aversive conditioning to a compound odor stimulus and its components in a terrestrial mollusc. Zoo Sci. 16:1999;879-883.
134. Serizawa S., Ishii T., Nakatani H., Tsuboi A., Nagawa F., Asano M., Sudo K., Sakagami J., Sakano H., Ijiri T., Matsuda Y., Suzuki M., Yamamori T., Iwakura Y., Sakano H. Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci. 3:2000;687-693.
135. Shepherd G.M., Greer C.A. Olfactory bulb. Shepherd G.M. The synaptic organization of the brain. 4th ed:1998;159-203 Oxford University Press, New York.
136. Sicard G. Olfactory discrimination of structurally related molecules: receptor cell responses to camphoraceous odorants. Brain Res. 326:1985;203-212.
137. Slotnick B.M., Bell G.A., Panhuber H., Laing D.G. Detection and discrimination of propionic acid after removal of its 2-DG identified major focus in the olfactory bulb: a psychophysical analysis. Brain Res. 762:1997;89-96.
138. Slotnick B.M., Graham S., Laing D.G., Bell G.A. Detection of propionic acid vapor by rats with lesions of olfactory bulb areas associated with high 2-DG uptake. Brain Res. 417:1987;343-346.
139. Slotnick B. Animal cognition and the rat olfactory system. Trends Cogn Sci. 5:2001;216-222.
140. Solomon G.E.A. Psychology of novice and expert wine talk. Am J Psychol. 103:1990;495-517.
141. Spors H., Grinvald A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron. 34:2002;301-315.
142. Staubli U., Fraser D., Faraday R., Lynch G. Olfaction and the data memory system in rats. Behav Neurosci. 101:1987;757-765.
143. Stevenson R.J. The acquisition of odour quality. Q J Exp Psychol. 54A:2001;561-578.
144. Stevenson R.J. Associative learning and odor quality perception: how sniffing an odor mixture can alter the smell of its parts. Learn Motiv. 32:2001;154-177.
145. Stevenson R.J. Perceptual learning with odors: implications for psychological accounts of odor quality perception. Psychonom Bull Rev. 8:2001;708-712.
146. Stevenson R.J., Boakes R.A., Prescott J. Changes in odor sweetness resulting from implicit learning of a simultaneous odor-sweetness association: an example of learned synesthesia. Learn Motiv. 29:1998;113-132.
147. Stevenson R.J., Boakes R.A. Sweet and sour smells: learned synesthesia between the senses of taste and smell. Spence C., Calvert G., Stein B. Handbook of multisensory processing. 2003;MIT Press, Boston. in press.
148. Stevenson R.J., Boakes R.A. A mnemonic theory of odor perception. Psychol Rev. 110:2003;340-364.
149. Stevenson RJ, Case TI, Boakes RA. Smelling what was there: acquired olfactory percepts are resistant to further modification. Learning and Motivation 2003;34:185-202.
150. Stevenson R.J., Prescott J. Judgments of chemosensory mixtures in memory. Acta Psychol. 95:1997;195-214.
151. Stevenson R.J., Prescott J., Boakes R.A. The acquisition of taste properties by odors. Learn Motiv. 26:1995;433-455.
152. Stevenson R.J., Prescott J., Boakes R.A. Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Sens. 24:1999;627-635.
153. Stopfer M., Bhagavan S., Smith B.H., Laurent G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature. 390:1997;70-74.
154. Stripling J.S., Patneau D.K., Gramlich C.A. Selective long-term potentiation in the pyriform cortex. Brain Res. 441:1988;281-291.
155. Sullivan R.M., Landers M., Yeaman B., Wilson D.A. Good memories of bad events in infancy. Nature. 407:2000;38-39.
156. Sullivan R.M., Taborsky-Barba S., Mendoza R., Itano A., Leon M., Cotman C.W., Payne T.F., Lott I. Olfactory classical conditioning in neonates. Pediatrics. 87:1991;511-518.
157. Sullivan S.L., Ressler K.J., Buck L.B. Spatial patterning and information coding in the olfactory system. Curr Opin Genet Dev. 5:1995;516-523.
158. Tanaka K. Mechanisms of visual object recognition studied in monkeys. Spatial Vision. 13:2000;147-163.
159. Timmermans J. Un nouvel etat mesomorphe, les cristaux organiques plastiques. J Chim Phys. 35:1938;331-344.
160. Tovee M.J., Rolls E.T., Ramachandran V.S. Rapid visual learning in neurones of the primate temporal visual cortex. NeuroReport. 7:1996;2757-2760.
161. Uchida N., Takahashi Y.K., Tanifuji M., Mori K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci. 3:2000;1035-1043.
162. Ueno Y. Cross-cultural study of odor perception in Sherpa and Japanese people. Chem Senses. 18:1993;352-353.
163. Valentincic T., Kralj J., Stenovec M., Koce A., Caprio J. The behavioral detection of binary mixtures of amino acids and their individual components by catfish. J Exp Biol. 203:2000;3307-3317.
164. 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. 79:1994;981-991.
165. Viana Di Prisco G., Freeman W.J. Odor-related bulbar EEG spatial pattern analysis during appetitive conditioning in rabbits. Behav Neurosci. 99:1985;964-978.
166. Vickers N.J., Christensen T.A., Hildebrand J.G. Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J Comp Neurol. 400:1998;35-56.
167. Walk R.D. Perceptual learning and the discrimination of wines. Psychonom Sci. 5:1966;57-58.
168. Wang H.W., Wysocki C.J., Gold G.H. Induction of olfactory receptor sensitivity in mice. Science. 260:1993;998-1000.
169. Watt R. Understanding vision. 1991;Academic Press, London.
170. White T.L. Olfactory memory: the long and short of it. Chem Sens. 23:1998;433-441.
171. Wilson D.A. Habituation of odor responses in the rat anterior piriform cortex. J Neurophysiol. 79:1998;1425-1440.
172. Wilson D.A. Synaptic correlates of odor habituation in the rat anterior piriform cortex. J Neurophysiol. 80:1998;998-1001.
173. Wilson D.A. Odor specificity of habituation in the rat anterior piriform cortex. J Neurophysiol. 83:2000;139-145.
174. Wilson D.A. A comparison of odor receptive field plasticity in the rat olfactory bulb and anterior piriform cortex. J Neurophysiol. 84:2000;3036-3042.
175. Wilson D.A. Scopolamine enhances generalization between odor representations in rat olfactory cortex. Learn Mem. 8:2001;279-285.
176. Wilson D.A. Receptive fields in the rat piriform cortex. Chem Senses. 26:2001;577-584.
177. Wilson DA. Rapid, experience-induced enhancement in odorant discrimination by anterier piriform cortex neurons. Journal of Neurophysiology 2003; in press.
178. Wilson D.A., Stevenson R.J. The fundamental role of memory in olfactory perception. Trends Neurosci. 2003;. in press.
179. Wilson D.A., Sullivan R.M. Neurobiology of associative learning in the neonate: Early olfactory learning. Behav Neural Biol. 61:1994;1-18.
180. 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. 7:1987;3154-3162.
181. Wysocki C.J., Beauchamp G.K. Ability to smell androstenone is genetically determined. Proc Natl Acad Sci USA. 81:1984;4899-4902.
182. Wysocki C.J., Dorries K.M., Beauchamp G.K. Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc Natl Acad Sci USA. 86:1989;7976-7978.
183. Xu F., Greer C.A., Shepherd G.M. Odor maps in the olfactory bulb. J Comp Neurol. 422:2000;489-495.
184. Yee K.K., Wysocki C.J. Odorant exposure increases olfactory sensitivity: olfactory epithelium is implicated. Physiol Behav. 72:2001;705-711.
185. Yokoi M., Mori K., Nakanishi S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA. 92:1995;3371-3375.
186. Young T.A., Wilson D.A. Frequency-dependent modulation of inhibition in the rat olfactory bulb. Neurosci Lett. 276:1999;65-67.
187. Youngentob S.L., Kent P.F. Enhancement of odorant-induced mucosal activity patterns in rats trained on an odorant identification task. Brain Res. 670:1995;82-88.
188. Zhao H., Ivic L., Otaki J.M., Hashimoto M., Mikoshiba K., Firestein S. Functional expression of a mammalian odorant receptor. Science. 279:1998;237-242.
189. Zou Z., Horowitz L.F., Montmayeur J.P., Snapper S., Buck L.B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature. 414:2001;173-179.