Oscillatory dynamics and information processing in olfactory systems

Journal of Experimental Biology

Volumn 202, Issue 14, 1999, Pages 1855-1864

  Gelperin, Alan ^a  

^a LUCENT TECHNOLOGIES   (United States)

Author keywords

Information processing; Memory; Odour discrimination; Olfaction; Olfactory dynamics

Indexed keywords

EID: 0032796698     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (124)

1. Abel, T. and Kandel, E. R. (1998). Positive and negative regulatory mechanisms that mediate long term memory storage. Brain Res. Rev. 26, 360-378.
2. Ache, B. W. (1991). Phylogeny of smell and taste. In Smell and Taste in Health and Disease (ed. T. V. Getchell, R. L. Doty, L. M. Bartoshuk and J. B. Snow), pp. 3-18. New York: Raven Press.
3. Adrian, E. D. (1942). Olfactory reactions in the brain of the hedgehog. J. Physiol., Lond. 100, 459-473.
4. Baker, T. C., Fadamiro, H. Y. and Cosse, A. A. (1998). Moth uses fine tuning for odour resolution. Nature 393, 530.
5. Bernocchi, G., Vignola, C., Scherini, E., Necchi, D. and Pisu, M. B. (1998). Bioactive peptides and serotonin immunocytochemistry in the cerebral ganglia of hibernating Helix aspersa. J. Exp. Zool. 280, 354-367.
6. Bozza, T. C. and Kauer, J. S. (1998). Odorant response properties of convergent olfactory receptor neurons. J. Neurosci. 18, 4560-4569.
7. Brezina, V., Orekhova, I. V. and Weiss, K. R. (1996). Functional uncoupling of linked neurotransmitter effects by combinatorial convergence. Science 273, 806-810.
8. Brezina, V. and Weiss, K. R. (1997). Analyzing the functional consequences of transmitter complexity. Trends Neurosci. 20, 538-543.
9. Broillet, M. C. and Firestein, S. (1996). Direct activation of the olfactory cyclic nucleotide gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16, 377-385.
10. 2+ channel. Neuron 18, 951-958.
11. Brunjes, P. C. (1994). Unilateral naris closure and olfactory system development. Brain Res. Rev. 19, 146-160.
12. Buck, L. (1996). Information coding in the vertebrate olfactory bulb. Annu. Rev. Neurosci. 19, 517-544.
13. 14C-2-deoxyglucose autoradiography. J. Neurosci. 5, 2930-2939.
14. Chase, R. and Rieling, J. (1986). Autoradiographic evidence for receptor cell renewal in the olfactory epithelium of a snail. Brain Res. 384, 232-239.
15. Chase, R. and Tolloczko, B. (1986). Synaptic glomeruli in the olfactory system of a snail. Cell Tissue Res. 246, 567-573.
16. Chase, R. and Tolloczko, B. (1993). Tracing neural pathways in snail olfaction: From the tip of the tentacles to the brain and beyond. Microsc. Res. Tech. 24, 214-230.
17. Cinelli, A. R., Hamilton, K. A. and Kauer, J. S. (1995). Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J. Neurophysiol. 73, 2053-2071.
18. Classen, J., Gerloff, C., Honda, M. and Hallett, M. (1998). Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. J. Neurophysiol. 79, 1567-1573.
19. Cooke, I. R. C., Edwards, S. L. and Anderson, C. R. (1994). The distribution of NADPH-diaphorase activity and immunoreactivity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa. Cell Tissue Res. 277, 565-572.
20. Cooke, I. and Gelperin, A. (1988). Distribution of FMRFamide-like immunoreactivity in the nervous system of the slug Limax maximus. Cell Tissue Res. 253, 69-76.
21. Corotto, F. S., Henegar, J. R. and Maruniak, J. A. (1994). Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neurosci. 61, 739-744.
22. Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M. and Snyder, S. H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88, 7797-7801.
23. Decharms, R. C. and Merzenich, M. M. (1996). Primary cortical representation of sounds by the coordination of action potential timing. Nature 381, 610-613.
24. Delaney, K. R., Gelperin, A., Fee, M. S., Flores, J. A., Gervais, R., Tank, D. W. and Kleinfeld, D. (1994). Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc. Natl. Acad. Sci. USA 91, 669-673.
25. Delaney, K. R. and Hall, J. B. (1995). An in vitro preparation of frog nose and brain for the study of odour-evoked oscillatory activity. J. Neurosci. Meth. 68, 193-202.
26. Donoghue, J. P., Sanes, J. N., Hatsopoulos, N. G. and Gaal, G. (1998). Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 79, 159-173.
27. Dynes, J. L. and Ngai, J. (1998). Pathfinding of olfactory neuron axons to stereotyped glomerular targets revealed by dynamic imaging in living zebrafish embryos. Neuron 20, 1081-1091.
28. Elekes, K., Hernadi, L., Muren, J. E. and Nässel, D. R. (1994). Peptidergic neurons in the snail Helix pomatia: Distribution of neurons in the central and peripheral nervous system that react with an antibody raised against an insect neuropeptide, leucokinin I. J. Comp. Neurol. 341, 257-272.
29. Elekes, K. and Nässel, D. R. (1990). Distribution of FMRFamide-like immunoreactive neurons in the central nervous system of the snail Helix pomatia. Cell Tissue Res. 262, 177-190.
30. Elekes, K. and Nässel, D. R. (1994). Tachykinin-related neuropeptides in the central nervous system of the snail, Helix pomatia: an immunocytochemical study. Brain Res. 661, 223-236.
31. Elekes, K. and Nässel, D. R. (1999). Pigment-dispersing hormone-like neurons in the central nervous system of gastropods, Helix and Lymnaea. Cell Tissue Res. (in press).
32. Elekes, K., Stefano, G. B. and Carpenter, D. O. (1993). Enkephalin-like immunoreactive neurons in the central nervous system of gastropods (Helix pomatia, Lymnaea stagnalis, Aplysia californica): a comparative immunocytochemical study. Cell Tissue Res. 272, 329-341.
33. Ermentrout, B., Flores, J. and Gelperin, A. (1998). Minimal model of oscillations and waves in the Limax olfactory lobe with tests of the model's predictive power. J. Neurophysiol. 79, 2677-2689.
34. Ermentrout, B. and Gelperin, A. (1998). Model for olfactory discrimination and learning in the Limax procerebral lobe incorporating oscillatory dynamics and wave propagation. Soc. Neurosci. Abstr. 24, 652.
35. Freeman, W. J. (1991). Nonlinear dynamics in olfactory information processing. In Olfaction: A Model System for Computational Neuroscience (ed. J. L. Davis and H. Eichenbaum), pp. 225-249. Cambridge, MA: MIT Press.
36. Freeman, W. J. and Schneider, W. S. (1982). Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiol. 19, 44-56.
37. Friedrich, A. and Teyke, T. (1998). Identification of stimuli and input pathways mediating food-attraction conditioning in the snail, Helix. J. Comp. Physiol. A 183, 247-254.
38. Friedrich, R. W. and Korsching, S. I. (1997). Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737-752.
39. Gelperin, A. (1975). Rapid food-aversion learning by a terrestrial mollusk. Science 189, 567-570.
40. Gelperin, A. (1994). Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369, 61-63.
41. Gelperin, A. and Flores, J. (1997). Vital staining from dye-coated microprobes identifies new olfactory interneurons for optical and electrical recording. J. Neurosci. Meth. 72, 97-108.
42. Gelperin, A., Flores, J. and Teyke, T. (1998). Olfactory oscillations enable odor discrimination by the Limax nose-brain preparation. Soc. Neurosci. Abstr. 24, 653.
43. Gelperin, A., Kleinfeld, D., Denk, W. and Cooke, I. R. C. (1996). Oscillations and gaseous oxides in invertebrate olfaction. J. Neurobiol. 30, 110-122.
44. Gelperin, A., Rhines, L., Flores, J. and Tank, D. (1993). Coherent network oscillations by olfactory interneurons: Modulation by endogenous amines. J. Neurophysiol. 69, 1930-1939.
45. Gelperin, A. and Tank, D. W. (1990). Odor-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345, 437-440.
46. Gerard, R. W. and Young, J. Z. (1937). Electrical activity of the central nervous system of the frog. Proc. R. Soc. B 122, 343-352.
47. Gervais, R., Kleinfeld, D., Delaney, K. R. and Gelperin, A. (1996). Central and reflex neuronal responses elicited by odor in a terrestrial mollusc. J. Neurophysiol. 76, 1327-1339.
48. Gray, C. M. (1994). Synchronous oscillations in neuronal systems: Mechanisms and functions. J. Comput. Neurosci. 1, 11-38.
49. Gray, C. M. and DiPrisco, G. V. (1997). Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J. Neurosci. 17, 3239-3253.
50. Harzsch, S., Miller, J., Benton, J. and Beltz, B. (1999). From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum. J. Neurosci. 19, 3472-3485.
51. Heinbockel, T., Kloppenberg, P. and Hildebrand, J. G. (1998). Pheromone-evoked potentials and oscillations in the antennal lobes of the sphinx moth Manduca sexta. J. Comp. Physiol. A 182, 703-714.
52. Hernadi, L., Juhos, S. and Elekes, K. (1993). Distribution of dopamine-immunoreactive and tyrosine-hydroxylase immunoreactive neurons in the central nervous system of Helix pomatia. Cell Tissue Res. 274, 503-513.
53. Hernadi, L., Teranno, Y., Muneoka, Y. and Kiss, T. (1995). Distribution of catch-relaxing peptide (CARP)-like immunoreative neurons in the central and peripheral nervous system of Helix pomatia. Cell Tissue Res. 280, 335-348.
54. Hildebrand, J. G. and Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595-631.
55. Hope, B. T., Michael, G. J., Knigge, K. M. and Vincent, S. R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA 88, 2811-2814.
56. Hopfield, J. F. and Gelperin, A. (1989). Differential conditioning to a compound stimulus and its components in the terrestrial mollusc Limax maximus. Behav. Neurosci. 103, 274-293.
57. Hopfield, J. J. (1991). Olfactory computation and object perception. Proc. Natl. Acad. Sci. USA 88, 6462-6466.
58. Hopfield, J. J. (1995). Pattern recognition compulation using action potential timing for stimulus representation. Nature 376, 33-36.
59. Hopkins, D. A., Steinbusch, H. W. M., Markerink-Van Ittersum, M. and De Vente, J. (1996). Nitric oxide synthase, cGMP and NO-mediated cGMP production in the olfactory bulb of the rat. J. Comp. Neurol. 375, 641-658.
60. Huang, S., Kerschbaum, H. H., Engel, E. and Hermann, A. (1997). Biochemical characterization and histochemical localization of nitric oxide synthase in the nervous system of the snail, Helix pomatia. J. Neurochem. 69, 2516-2528.
61. Huang, S., Kerschbaum, H. H. and Hermann, A. (1998). Nitric oxide-mediated cGMP synthesis in Helix neural ganglia. Brain Res. 780, 329-336.
62. Isaacson, J. S. and Strowbridge, B. W. (1998). Olfactory reciprocal synapses: Dendritic signaling in the CNS. Neuron 20, 749-761.
63. Joerges, J., Küttner, A., Galizia, C. G. and Menzel, R. (1997). Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285-288.
64. Johnson, B. A. and Leon, M. (1996). Spatial distribution of [C-14]2-deoxyglucose uptake in the glomerular layer of the rat olfactory bulb following early odor preference learning. J. Comp. Neurol. 376, 557-566.
65. Kaufmann, W., Kerschbaum, H. H., Hauserkronberger, C., Hacker, G. W. and Hermann, A. (1995). Distribution and seasonal variation of vasoactive intestinal (VIP)-like peptides in the nervous system of Helix pomatia. Brain Res. 695, 125-136.
66. Kawahara, S., Toda, S., Suzuki, Y., Watanabe, S. and Kirino, Y. (1997). Comparative study on neural oscillation in the procerebrum of the terrestrial slugs Incilaria bilineata and Limax marginatus. J. Exp. Biol. 200, 1851-1861.
67. Kendrick, K. M., Guevara-Guzman, R., Zorrilla, J., Hinton, M. R., Broad, K. D., Mimmack, M. and Ohkura, S. (1997). Formation of olfactory memories mediated by nitric oxide. Nature 388, 670-674.
68. Kim, U., Bal, T. and McCormick, D. A. (1995). Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. J. Neurophysiol. 74, 1301-1323.
69. Kimura, T., Suzuki, H., Kono, E. and Sekiguchi, T. (1998). Mapping of interneurons that contribute to food aversion conditioning in the slug brain. Learning & Memory 4, 376-388.
70. Kleinfeld, D., Delaney, K. R., Fee, M. S., Flores, J. A., Tank, D. W. and Gelperin, A. (1994). Dynamics of propagating waves in the olfactory network of a terrestrial mollusc: An electrical and optical study. J. Neurophysiol. 72, 1402-1419.
71. Kohonen, T. and Hari, R. (1999). Where the abstract feature maps of the brain might come from. Trends Neurosci. 22, 135-139.
72. Laurent, G. (1996). Odor images and tunes. Neuron 16, 473-476.
73. Laurent, G. (1997). Olfactory processing: maps, time and codes. Curr. Opin. Neurobiol. 7, 547-553.
74. Laurent, G., Wehr, M. and Davidowitz, H. (1996). Odour encoding by temporal sequences of firing in oscillating neural assemblies. J. Neurosci. 16, 3837-3847.
75. Leitch, B. and Laurent, G. (1996). GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J. Comp. Neurol. 372, 487-514.
76. Lin, D. M. and Ngai, J. (1999). Development of the vertebrate main olfactory system. Curr. Opin. Neurobiol. 9, 74-78.
77. Lin, Y. Q. and Bennett, M. R. (1994). Nitric-oxide modulation of quantal secretion in chick ciliary ganglia. J. Physiol., Lond. 481, 385-394.
78. Lois, C. and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
79. Lu, X. C. M. and Slotnick, B. M. (1998). Olfaction in rats with extensive lesions of the olfactory bulbs: Implications for odor coding. Neurosci. 84, 849-866.
80. MacLeod, K. and Laurent, G. (1996). Distinct mechanisms for synchronization and temporal patterning of odor-coding assemblies. Science 274, 976-979.
81. Magdelaine, S., Mansuit, P., Marchand, C. R. and Richardson, J. (1991). Growth and SRIF-like substances in the snail Helix aspersa maxima fed with an arginin-enriched food at different times of a short daily photoperiod. Comp. Biochem. Physiol. 99A, 429-435.
82. Marchand, C. R., Griffond, B. and MouColard, C. (1991). Distribution of methionine-enkephalin-like and FMRFamide-like immunoreactivities in the central nervous system (including dorsal bodies) of the snail Helix aspersa Müller. Zool. Sci. 8, 905-913.
83. Marder, E. (1998). From biophysics to models of network function. Annu. Rev. Neurosci. 21, 25-45.
84. McCarragher, G. and Chase, R. (1985). Quantification of ultrastructural symmetry at molluscan chemical synapses. J. Neurobiol. 16, 69-74.
85. Menzel, R. and Müller, U. (1996). Learning and memory in honeybees: From behavior to neural substrate. Annu. Rev. Neurosci. 19, 379-404.
86. Meredith, M. (1986). Patterned response to odor in mammalian olfactory bulb: the influence of intensity. J. Neurophysiol. 56, 572-597.
87. Mitra, P. P. and Pesaran, B. (1999). Analysis of dynamic brain imaging data. Biophys. J. 76, 691-708.
88. Moroz, L. L., Gillette, R. and Sweedler, J. V. (1999). Single-cell analysis of nitrergic neurons in simple nervous systems. J. Exp. Biol. 202, 333-341.
89. Müller, U. (1996). Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16, 541-549.
90. Murthy, V. N. and Fetz, E. E. (1996). Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J. Neurophysiol. 76, 3949-3967.
91. Najbauer, J. and Leon, M. (1995). Olfactory experience modulates apoptosis in the developing olfactory bulb. Brain Res. 674, 245-251.
92. Osborne, N. N. and Cottrell, G. A. (1971). Distribution of biogenic amines in the slug Limax maximus. Z. Zellforsch. 112, 15-30.
93. Peschel, M., Straub, V. and Teyke, T. (1996). Consequences of food-attraction conditioning in Helix: A behavioral and electrophysiological study. J. Comp. Physiol. 178, 317-327.
94. Poteryaev, D. A., Zakharov, I. S., Balaban, P. M. and Belyavsky, A. V. (1998). A novel neuropeptide precursor gene is expressed in the terrestrial snail central nervous system by a group of neurons that control mating behavior. J. Neurobiol. 35, 183-197.
95. Poteryaev, D. A., Zakharov, I. S., Balaban, P. M., Uvarov, P. N. and Belyavsky, A. V. (1997). Characterization of a cDNA clone encoding pedal peptide in the terrestrial snail. NeuroReport 8, 3631-3635.
96. Prechtl, J., Cohen, L. B., Pesaran, B., Mitra, P. P. and Kleinfeld, D. (1997). Visual stimuli induce waves of electrical activity in turtle cortex. Proc. Natl. Acad. Sci. USA 94, 7621-7626.
97. Rall, W., Shepherd, G. M., Reese, T. S. and Brightman, M. W. (1966). Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44-56.
98. 3H]-2-deoxyglucose autoradiography in a molluscan nervous system. Brain Res. 208, 416-420.
99. Renteria, R. C. and Constantine-Paton, M. (1996). Exogenous nitric oxide causes collapse of retinal ganglion cell axonal growth cones in vitro. J. Neurobiol. 29, 415-428.
100. Rhines, L., Sokolove, P., Flores, J., Tank, D. W. and Gelperin, A. (1993). Cultured olfactory interneurons from Limax maximus: Optical and electrophysiological studies of transmitter-evoked responses. J. Neurophysiol. 69, 1940-1947.
101. Ribary, U., Joannides, A. A., Singh, K. D., Hasson, R., Bolton, J. P. R., Lado, F., Mogilner, A. and Llinas, R. (1991). Magnetic field tomography of coherent thalamocortical 40 Hz oscillations in humans. Proc. Natl. Acad. Sci. USA 88, 11037-11041.
102. Sahley, C. L. (1990). The behavioral analysis of associative learning in the terrestrial mollusc Limax maximus: The importance of interevent relationships. In Connectionist Modeling and Brain Function: The Developing Interface (ed. S. Hanson and C. Olson), pp. 36-73. Cambridge, MA: MIT Press.
103. Sánchez-Alvarez, M., León-Olea, M., Talavera, E., Pellicer, F., Sánchez-Islas, E. and Martínez-Lorenzana, G. (1994). Distribution of NADPH-diaphorase in the perioesophageal ganglia of the snail, Helix aspersa. Neurosci. Lett. 169, 51-55.
104. 3H]-2-deoxyglucose in single molluscan neurones. Nature 287, 449-451.
105. Senseman, D. M. (1996). High-speed optical imaging of afferent flow through rat olfactory bulb slices: Voltage-sensitive dye signals reveal periglomerular cell activity. J. Neurosci. 16, 313-324.
106. Shepherd, G. M. and Greer, C. A. (1990). Olfactory bulb. In The Synaptic Organization of the Brain (ed. G. M. Shepherd), pp. 133-169. New York: Oxford University Press.
107. Shipley, M. T. and Ennis, M. (1995). Functional organization of olfactory system. J. Neurobiol. 30, 123-176.
108. Singer, W. and Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586.
109. Stopfer, M., Bhagavan, S., Smith, B. H. and Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70-74.
110. Tank, D. W., Gelperin, A. and Kleinfeld, D. (1994). Odors, oscillations and waves: Does it all compute? Science 265, 1819-1820.
111. Technau, G. M. (1984). Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J. Neurogenet. 1, 113-126.
112. Teyke, T. (1996). Nitric oxide, but not serotonin, is involved in acquisition of food-attraction conditioning in the snail Helix pomatia. Neurosci. Lett. 206, 29-32.
113. Teyke, T. and Gelperin, A. (1999). Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. NeuroReport 10, 1061-1068.
114. Vickers, N. J., Christensen, T. A. and Hildebrand, J. G. (1998) Combinatorial odor discrimination in the brain: Attractive and antagonistic odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400, 35-56.
115. Wang, F., Nemes, A., Mendelsohn, M. and Axel, R. (1998). Odorant receptors govern the formation of a precise topographic map. Cell 93, 47-60.
116. Watanabe, S., Kawahara, S. and Kirino, Y. (1997). Glutamate responses of procerebral neurons of the terrestrial slug Limax marginatus. Soc. Neurosci. Abstr. 23, 1824.
117. Watanabe, S., Kawahara, S. and Kirino, Y. (1998). Morphological characterization of the bursting and nonbursting neurones in the olfactory centre of the terrestrial slug Limax marginatus. J. Exp. Biol. 201, 925-930.
118. Wehr, M. and Laurent, G. (1996). Odor encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162-166.
119. Wu, J. Y., Lam, Y. W., Falk, C. X., Cohen, L. B., Fang, J., Loew, L., Prechtl, J. C., Kleinfeld, D. and Tsau, Y. (1998). Voltage-sensitive dyes for monitoring multineuronal activity in the intact central nervous system. Histochem. J. 30, 169-187.
120. Yamane, T. and Gelperin, A. (1987). Aminergic and peptidergic amplification of intracellular cyclic AMP levels in a molluscan neural network. Cell. Mol. Neurobiol. 7, 291-301.
121. Yamane, T., Oestericher, A. B. and Gelperin, A. (1989). Serotonin-stimulated biochemical events in the procerebrum of Limax. Cell. Mol. Neurobiol. 9, 447-459.
122. Yokoi, M., Mori, K. and Nakanishi, S. (1995). Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92, 3371-3375.
123. Zakharov, I. S., Hayes, N. L., Ierusalimsky, V. N., Nowakowski, R. S. and Balaban, P. M. (1998). Postembryonic neuronogenesis in the procerebrum of the terrestrial snail, Helix lucorum. J. Neurobiol. 35, 271-276.
124. Zs.-Nagy, I. and Sakharov, D. A. (1970). The fine structure of the procerebrum of pulmonate molluscs, Helix and Limax. Tissue & Cell 2, 399-411.