Neural substrates of memory: From synapse to system

Journal of Neurobiology

Volumn 54, Issue 1, 2003, Pages 238-253

  Dubnau, Josh ^a   Chiang, Ann Shyn ^b   Tully, Tim ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Behavioral analyses; Memory; Neural substrates; Theoretical modeling

Indexed keywords

BEHAVIOR GENETICS; BEHAVIORAL SCIENCE; DROSOPHILA; LONG TERM MEMORY; MEMORY CONSOLIDATION; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SHORT TERM MEMORY; SYNAPTIC TRANSMISSION; THEORETICAL MODEL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; DROSOPHILA MELANOGASTER; MEMORY; NERVOUS SYSTEM; NEURONAL PLASTICITY; NEURONS; SYNAPSES;

EID: 0037218320     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10170     Document Type: Review

References (134)

1. Aksay E, Gamkrelidze G, Seung HS, Baker R, Tank DW. 2001. In vivo intracellular recording and perturbation of persistent activity in a neural integrator. Nat Neurosci 4:184-193.
2. Allweis C. 1991. The congruity of rat and chick multiphasic memory-consolidation models. In: Andrew RJ, editor. Neural and Behavioural Plasticity. New York: Oxford University Press, p 370-393.
3. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER. 2000. Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1: 11-20.
4. Barrionuevo G, Brown TH. 1983. Associative long-term potentiation in hippocampal slices. Proc Natl Acad Sci USA 80:7347-7351.
5. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER. 1995. Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979-992.
6. Bear MF. 1999. Homosynaptic long-term depression: A mechanism for memory? Proc Natl Acad Sci USA 96: 9457-9458.
7. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. 2001. Synaptic plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning. Learn Mem 8:229-242.
8. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
9. Bliss TV, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.
10. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
11. Byrne JH, Kandel ER. 1996. Presynaptic facilitation revisited: State and time dependence. J Neurosci 16:425-435.
12. Chain DG, Hegde AN, Yamamoto N, Liu-Marsh B, Schwartz JH. 1995. Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron-specific function of the ubiquitin system in Aplysia. J Neurosci 15:7592-7603.
13. Chen C, Kim JJ, Thompson RF, Tonegawa S. 1996. Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110:1177-1180.
14. Cheng Y, Endo K, Wu K, Rodan AR, Heberlein U, Davis RL. 2001. Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105:757-768.
15. Chiang AS, Liu YC, Chiu SL, Hu SH, Huang CY, Hsieh CH. 2001. Three-dimensional mapping of brain neuropils in the cockroach, Diploptera punctata. J Comp Neurol 440:1-11.
16. Connolly JB, Tully T. 1998. Integrins: A role for adhesion molecules in olfactory memory. Curr Biol 8:R386-R389.
17. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M, Tully T, O'Kane CJ. 1996. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-2107.
18. Dash PK, Hochner B, Kandel ER. 1990. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721.
19. Davis HP, Squire LR. 1984. Protein synthesis and memory: A review. Psychol Bull 96:518-559.
20. Davis S, Butcher SP, Morris RG. 1992. The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J Neurosci 12:21-34.
21. de Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
22. de Bruyne M, Foster K, Carlson JR. 2001. Odor coding in the Drosophila antenna. Neuron 30:537-552.
23. DeZazzo J, Tully T. 1995. Dissection of memory formation: From behavioral pharmacology to molecular genetics. Trends Neurosci 18:212-218.
24. DeZazzo J, Sandstrom D, de Belle S, Velinzon K, Smith P, Grady L, DelVecchio M, Ramaswami M, Tully T. 2000. Nalyot, a mutation of the Drosophila myb-related Adfl transcription factor, disrupts synapse formation and olfactory memory. Neuron 27:145-158.
25. DeZazzo J, Xia S, Christensen J, Velinzon K, Tully T. 1999. Developmental expression of an amn(+) transgene rescues the mutant memory defect of amnesiac adults. J Neurosci 19:8740-8746.
26. Drier EA, Tello MK, Cowan M, Wu P, Blace N, Sacktor TC, Yin JC. 2002. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nat Neurosci 5:316-324.
27. Dubnau J, Tully T. 2001. Functional anatomy: From molecule to memory. Curr Biol 11:R240-R243.
28. Dubnau J, Grady L, Kitamoto T, Tully T. 2001. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411:476-480.
29. Dubnau J, Tully T. 1998. Gene discovery in Drosophila: New insights for learning and memory. Annu Rev Neurosci 21:407-444.
30. Durstewitz D, Seamans JK, Sejnowski TJ. 2000. Neurocomputational models of working memory. Nat Neurosci (Suppl) 3:1184-1191.
31. Erber J. 1976. Retrograde amnesia in honeybees (Apis mellifera carnica). J Comp Physiol Psychol 90:41-46.
32. Faber T, Joerges J, Menzel R. 1999. Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2:74-78.
33. Feany MB, Quinn WG. 1995. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268:869-873.
34. Folkers E, Drain P, Quinn WG. 1993. Radish, a Drosophila mutant deficient in consolidated memory. Proc Natl Acad Sci USA 90:8123-8127.
35. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ. 1998. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112:863-874.
36. Fuster JM. 1995. Memory in the cortex of the primate. Biol Res 28:59-72.
37. Galluscio EH. 1971. Retrograde amnesia induced by electroconvulsive shock and carbon dioxide anesthesia in rats: An attempt to stimulate recovery. J Comp Physiol Psychol 75:136-140.
38. Gigg J, Patterson TA, Rose SP. 1994. Increases in neuronal bursting recorded from the chick lobus parolfactorius after training are both time-dependent and memory-specific. Eur J Neurosci 6:313-319.
39. Gilbert DB, Patterson TA, Rose SP. 1991. Dissociation of brain sites necessary for registration and storage of memory for a one-trial passive avoidance task in the chick. Behav Neurosci 105:553-561.
40. Glanzman DL. 1995. The cellular basis of classical conditioning in Aplysia californica - Its less siple than you think. Trends Neurosci 18:30-36.
41. Gronenberg W. 1987. Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. Exp Biol 46:115-125.
42. Grotewiel MS, Beck CD, Wu KH, Zhu XR, Davis RL. 1998. Integrin-mediated short-term memory in Drosophila. Nature 391:455-460.
43. Grunbaum L, Muller U. 1998. Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J Neurosci 18:4384-4392.
44. Guzowski JF, McGaugh JL. 1997. Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci USA 94:2693-2698.
45. Hammer M, Menzel R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146-156.
46. Han PL, Meller V, Davis RL. 1996. The Drosophila brain revisited by enhancer detection. J Neurobiol 31:88-102.
47. Hawkins RD. 1984. A cellular mechanism of classical conditioning in Aplysia. J Exp Biol 112:113-128.
48. Hebb DO. 1949. The Organization of Behavior. New York: John Wiley and Sons.
49. Hinton GE. 2000. Computation by neural networks. Nat Neurosci (Suppl) 3:1170.
50. Huang YY, Kandel ER, Varshavsky L, Brandon EP, Qi M, Idzerda RL, McKnight GS, Bourtchouladze R. 1995. A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83:1211-1222.
51. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ. 1998. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5:52-77.
52. Jefferis GS, Marin EC, Watts RJ, Luo L. 2002. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr Opin Neurobiol 12: 80-86.
53. Josselyn SA, Shi C, Carlezon WA, Jr., Neve RL, Nestler EJ, Davis M. 2001. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404-2412.
54. Kandel ER, Spencer WA. 1968. Cellular neurophysiological approaches in the study of learning. Physiol Rev 48:65-134.
55. Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ. 2002. CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355.
56. Kim J, Moriyama EN, Warr CG, Clyne PJ, Carlson JR. 2000. Identification of novel multi-transmembrane proteins from genomic databases using quasi-periodic structural properties. Bioinformatics 16:767-775.
57. Kitamoto T. 2001. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92.
58. Lamprecht R, Hazvi S, Dudai Y. 1997. cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J Neurosci 17:8443-8450.
59. Laurent G, Naraghi M. 1994. Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14: 2993-3004.
60. Lei H, Christensen TA, Hildebrand JG. 2002. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557-565.
61. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J. 2002. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416:90-94.
62. Levy WB, Steward O. 1979. Synapses as associative memory elements in the hippocampal formation. Brain Res 175:233-245.
63. Li W, Tully T, Kalderon D. 1996. Effects of a conditional Drosophila PKA mutant on olfactory learning and memory. Learn Mem 2:320-333.
64. Li Y, Strausfeld NJ. 1997. Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol 387:631-650.
65. Liu L, Wolf R, Ernst R, Heisenberg M. 1999. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400:753-756.
66. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC. 1997. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA 1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196-5205.
67. Malenka RC, Nicoll RA. 1999. Long-term potentiation - A decade of progress? Science 285:1870-1874.
68. Malinow R, Mainen ZF, Hayashi Y. 2000. LTP mechanisms: From silence to four-lane traffic. Curr Opin Neurobiol 10:352-357.
69. Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
70. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
71. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK. 1999. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967-977.
72. McGuire SE, Le PT, Davis RL. 2001. The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333.
73. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390:607-611.
74. McNaughton BL, Douglas RM, Goddard GV. 1978. Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents. Brain Res 157:277-293.
75. Menzel R. 2001. Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53-62.
76. Milner B. 1972. Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg 19:421-446.
77. Mitsuno K, Sasa M, Ishihara K, Ishikawa M, Kikuchi H. 1994. LTP of mossy fiber-stimulated potentials in CA3 during learning in rats. Physiol Behav 55:633-638.
78. Mizunami M, Okada R, Li Y, Strausfeld NJ. 1998. Mushroom bodies of the cockroach: Activity and identities of neurons recorded in freely moving animals. J Comp Neurol 402:501-519.
79. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S. 1986. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
80. Morris RG. 1989. Synaptic plasticity and learning: Selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 9:3040-3057.
81. Morris RG, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
82. Muller U. 1999. Second messenger pathways in the honeybee brain: Immunohistochemistry of protein kinase A and protein kinase C. Microsc Res Technol 45:165-173.
83. Muller U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:159-168.
84. Muller U, Carew TJ. 1998. Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron 21:1423-1434.
85. Murphy GG, Glanzman DL. 1999. Cellular analog of differential classical conditioning in Aplysia: Disruption by the NMDA receptor antagonist DL-2-amino-5-phosphonovalerate. J Neurosci 19:10595-10602.
86. Nalbantoglu J, Tirado-Santiago G, Lahsaini A, Poirier J, Goncalves O, Verge G, Momoli F, Welner SA, Massicotte G, Julien JP, Shapiro ML. 1997. Impaired learning and LTP UP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387:500-505.
87. Pascual A, Preat T. 2001. Localization of long-term memory within the Drosophila mushroom body. Science 294: 1115-1117.
88. Patterson TA, Gilbert DB, Rose SP. 1990. Pre- and post-training lesions of the intermediate medial hyperstriatum ventrale and passive avoidance learning in the chick. Exp Brain Res 80:189-195.
89. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G. 2002. Oscillations and sparsening of odor representations in the mushroom body. Science 297:359-365.
90. Philip N, Acevedo SF, Skoulakis EM. 2001. Conditional rescue of olfactory learning and memory defects in mutants of the 14-3-3zeta gene leonardo. J Neurosci 21: 8417-8425.
91. Pinto S, Quintana DG, Smith P, Mihalek RM, Hou ZH, Boynton S, Jones CJ, Hendricks M, Velinzon K, Wohlschlegel JA, Austin RJ, Lane WS, Tully T, Dutta A. 1999. Latheo encodes a subunit of the origin recognition complex and disrupts neuronal proliferation and adult olfactory memory when mutant. Neuron 23:45-54.
92. Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER. 2002. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447-462.
93. Quinn WG, Dudai Y. 1976. Memory phases in Drosophila. Nature 262:576-577.
94. Rein K, Zockler M, Mader MT, Grubel C, Heisenberg M. 2002. The Drosophila standard brain. Curr Biol 12:227-231.
95. Rioult-Pedotti MS, Friedman D, Donoghue JP. 2000. Learning-induced LTP in neocortex. Science 290:533-536.
96. Rogan MT, Staubli UV, LeDoux JE. 1997. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607.
97. Rohrbough J, Pinto S, Mihalek RM, Tully T, Broadie K. 1999. Latheo, a Drosophila gene involved in learning, regulates functional synaptic plasticity. Neuron 23:55-70.
98. Rosay P, Armstrong JD, Wang Z, Kaiser K. 2001. Synchronized neural activity in the Drosophila memory centers and its modulation by amnesiac. Neuron 30:759-770.
99. Rybak J, Menzel R. 1998. Integrative properties of the Pel neuron, a unique mushroom body output neuron. Learn Mem 5:133-145.
100. Schacher S, Glanzman D, Barzilai A, Dash P, Grant SG, Keller F, Mayford M, Kandel ER. 1990. Long-term facilitation in Aplysia: Persistent phosphorylation and structural changes. Cold Spring Harb Symp Quant Biol 55: 187-202.
101. Scoville WB, Milner B. 2000. Loss of recent memory after bilateral hippocampal lesions, 1957. J Neuropsychiatr Clin Neurosci 12:103-113.
102. Skoulakis EM, Davis RL. 1996. Olfactory learning deficits in mutants for leonardo, a Drosophila gene encoding a 14-3-3 protein. Neuron 17:931-944.
103. Squire LR. 1992. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195-231.
104. Stopfer M, Laurent G. 1999. Short-term memory in olfactory network dynamics. Nature 402:664-668.
105. Strausfeld NJ. 1976. Atlas of an Insect Brain. New York: Springer-Verlag.
106. Strausfeld NJ, Li Y. 1999. Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies. J Comp Neurol 409:626-646.
107. Strauss R, Heisenberg M. 1993. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852-1861.
108. Sutton MA, Masters SE, Bagnall MW, Carew TJ. 2001. Molecular mechanisms underlying a unique intermediate phase of memory in Aplysia. Neuron 31:143-154.
109. Tang S, Guo A. 2001. Choice behavior of Drosophila facing contradictory visual cues. Science 294:1543-1547.
110. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY. 2002. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34:289-300.
111. Tully T, Quinn WG. 1985. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157:263-277.
112. Tully T, Bolwig G, Christensen J, Connolly J, DeZazzo J, Dubnau J, Jones C, Pinto S, Regulski M, Svedberg F, Velinzon K. 1996. Genetic dissection of memory in Drosophila. J Physiol Paris 90:383.
113. Tully T, Boynton S, Brandes C, Dura JM, Mihalek R, Preat T, Villella A. 1990. Genetic dissection of memory formation in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 55:203-211.
114. Tully T, Preat T, Boynton SC, Del Vecchio M. 1994. Genetic dissection of consolidated memory in Drosophila. Cell 79:35-47.
115. Villa AE, Fuster JM. 1992. Temporal correlates of information processing during visual short-term memory. Neuroreport 3:113-116.
116. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
117. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
118. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG. 2000. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805-813.
119. Waddell S, Quinn WG. 2001. Flies, genes, and learning. Annu Rev Neurosci 24:1283-1309.
120. Wang XJ. 2001. Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24:455-463.
121. Wang Y, Wright NJ, Guo H, Xie Z, Svoboda K, Malinow R, Smith DP, Zhong Y. 2001. Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body. Neuron 29:267-276.
122. Wehr M, Laurent G. 1996. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384:162-166.
123. Weisskopf MG, Bauer EP, LeDoux JE. 1999. L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci 19:10512-10519.
124. Weissman A. 1967. Drugs and retrograde amnesia. Int Rev Neurobiol 10:167-198.
125. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
126. Xia S, Liu L, Feng C, Guo A. 1997. Drug disruption of short-term memory in Drosophila melanogaster. Pharmacol Biochem Behav 58:727-735.
127. Xia SZ, Feng CH, Guo AK. 1999. Temporary amnesia induced by cold anesthesia and hypoxia in Drosophila. Physiol Behav 65:617-623.
128. Yamada A, Sekiguchi T, Suzuki H, Mizukami A. 1992. Behavioral analysis of internal memory states using cooling-induced retrograde amnesia in Limax flavus. J Neurosci 12:729-735.
129. Yin JC, Del Vecchio M, Zhou H, Tully T. 1995. CREB as a memory modulator: Induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81:107-115.
130. Yin JC, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T. 1994. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.
131. Zars T, Fischer M, Schulz R, Heisenberg M. 2000a. Localization of a short-term memory in Drosophila. Science 288:672-675.
132. Zars T, Wolf R, Davis R, Heisenberg M. 2000b. Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: In search of the engram. Learn Mem 7:18-31.
133. Zhao WQ, Sedman GL, Gibbs ME, Ng KT. 1994. Effect of PKC inhibitors and activators on memory. Behav Brain Res 60:151-160.
134. Zipser D, Kehoe B, Littlewort G, Fuster J. 1993. A spiking network model of short-term active memory. J Neurosci 13:3406-3420.