medigraphic.com
ISSN 0185-3325 (Print)
Órgano Oficial del Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz

2002, Number 4

<< Back

Salud Mental 2002; 25 (4)

Understanding the neurobiological mechanisms of learning and memory: Memory systems of the brain, long term potentiation and synaptic plasticity Part III b

Leff P, Romo H, Matus M, Hernández A, Calva JC, Acevedo R, Torner C, Gutiérrez R, Anton B

Language: English
References: 135
Page: 78-94
PDF size: 580.68 Kb.


ABSTRACT

One of the central issues in neuroscience is concerned with the activity-dependent synaptic plasticity in learning and memory. In such context, changing the strength of synaptic activity between neurons has been widely accepted as the mechanism responsible by which memory traces are encoded and stored in the brain. Thus, the synaptic plasticity and memory hypothesis (SPM hypothesis) shows that activity-dependent synaptic plasticity is induced at appropiate synapses during memory formation, which is essential for information storage for the type of memory involved in the brain area where plasticity is detected or observed. Several criteria and experimental strategies are outlined, and used to investigate this hypothesis. Long-term potentiation (LTP) as an experimental model to study the cellular basis of learning and memory, is one of the most fascinating phenomena that have raised a great interest in neuroscience. LTP is a form of synaptic plasticity that is accepted as a cellular model for stabilization of synapses in several neurobiological events such as development, learning and memory. Defined as the increase in the strength of synaptic transmission observed after tetanic stimulation, this phenomenon can be measured from hours to days, and even outlast the stimulus that induced it over time. The role of LTP in learning has been a central issue in neuroscience, particularly in studies focused on the NMDA receptor-dependent forms of LTP. Thus, much of the experimental work performed in research regarding LTP has been aimed to investigate if LTP equals memory. This review described several properties of synaptic plasticity as well as the neural substrates where synaptic plasticity events are embedded in networks, so as to establish the processing of learning and memory formation.


REFERENCES

  1. ABRAHAM WC, MASON SE: Effects of the NMDA receptor/channels antagonists CPP and MK801 on hippocampal pyramidal field potentials and long term–potentiation in anesthetized rats. Brain Res, 462:40-46. 1998.

  2. ABRAHAM WC: Activity-dependent Regulation of Synaptic Plasticity (Metaplasticity) in the Hippocampus. In the Hippocampus: Functions and Clinical Relevance. Kato N (ed.). pp 15-34. Elsevier Sci, Amsterdam, 1996.

  3. ABRAHAM WC, BEAR MF: Metaplasticity: the plasticity of the synaptic plasticity. Trends Neurosci, 19:126-30. 1996.

  4. ARAI A, KESSLER M, XIAO P, AMBROS-INGERSON J, ROGERS, LYNCH G: A centrally active drug that modulates AMPA receptor gated currents. Brain Res, 638:343-46,1994.

  5. ARAI A, KESSLER M, XIAO P, AMBROS-INGERSON J, QUAN A, ROGERS G, LYNCH G: Effects of a centrally active benzoylpyrrolidine grug on AMPA receptors kinetics. Neuroscience, 75:573-85, 1996.

  6. ARTOLA A, BRÖCHER S, SINGER W: Different voltagedependent thresholds for inducing long-term depression and long-term potentiation slices of rat visual cortex. Nature, 347:69-72, 1990.

  7. BANNERMAN DM, CHAPMAN PF, KELLY PAT, BUTCHER SP, MORRIS RGM: Inhibition of nitric-oxide synthase does not prevent the induction of longterm potentiation in vivo. J Neurosci, 14:7415-25, 1994.

  8. BANNERMAN DM, GOOD MA, BUTCHER SP, RAMSAY M, MORRIS RG: Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378:182-86, 1995.

  9. BARNES CA: Involvement of LTP in memory: are we searching under the streetlight? Neuron, 15:751-54, 1995.

  10. BARNES CA, MCNAUGHTON BL: An age comparison of the rates of acquisition and forgetting of spatial information in relation to long–term enhancement of hippocampal synapses. Behav Neurosci, 99:1040-48, 1985.

  11. BASHIR ZI, BORTOLOTTO ZA, DAVIES CH, BERRETTA N, IRVING AJ et al.: Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature, 363:347-50, 1993.

  12. BASHIR ZI, COLLINGRIDGE GL: An investigation in the CA1 region of the hippocampus. Exp Brain Res, 100:437-43, 1994.

  13. BAUDRY M, DAVID JL, THOMPSON RF (eds.): Synaptic plasticity: Molecular and functional aspects. MIT Press, Cambridge, 1993.

  14. BEAR MF: Mechanism for a sliding synaptic modification threshold. Neuron, 15: 1-4, 1995.

  15. BLISS TVP, LOMO T: Long lasting of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J Physiol, 232:331-56, 1973.

  16. BLISS TV: Long-term potentiation. Science, 249(4972): 973, 1990.

  17. BLISS TV, ERRINGTON ML, LYNCH MA, WILLIAMS JH: Presynaptic mechanisms in hippocampal longterm potentiation. Cold Spring Harb Symp Quant Biol, 55:119-29, 1990.

  18. BLISS TVP, COLLINGRIDGE GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361:31-39, 1993.

  19. BORDI F, MARCON C, CHIAMULERA C, REGGIANI A: Effects of the metabotropic glutamate receptor antagonists MCPG on spatial and contex-specific learning. Neuropharmacology, 35:1557-65, 1996.

  20. BREAKWELL NA, ROWAN MJ, ANWYL R: (+)-MCPG blocks induction of LTP in the CA1 of rat hippocampus via agonists action at an mGluR group II receptor. J Neurophysiol, 79:1270-76, 1998.

  21. BUZSAKI G: Two-stage model of a memory-trace formation: a role for a ‘noisy’ brain states. Neuroscience, 31:551-70, 1989.

  22. BUTCHER SP, HAMBERGER A, MORRIS RGM: Intracerebral distribution of DL-2-amino-phosphonopentanoic acid (AP5) and the dissociation of different types of learning. Exp Brain Res, 83:521-26, 1991.

  23. CAIN DP, HARGREAVES EL, BOON F, DENNISON Z: An examination of the relations between hippocampal long-term potentiation, kindling afterdischarge, and place learning in the water maze. Hippocampus, 3:153- 63, 1993.

  24. CAIN DP, SAUCIER D, HALL J, HARGREAVES EL, BOON F: Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav Neurosci, 110:86-102, 1996.

  25. CASTRO CA, SILBERT LH, MCNAUGHTON BL, BARnes CA: Recovery of spatial learning deficits after decay of electrically induced synaptic enhancement in the hippocampus. Nature, 342:545-48, 1989.

  26. CHANCE FS et al.: Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci, 18:4785-4799, 1998.

  27. CHAPMAN PF, BELLAVANCE LL: Induction of longterm potentiation in the basolateral amygdala does not depend on NMDA receptor activation. Synapse, 11:310-18, 1992.

  28. CHAPMAN PF, WHITE GL, JONES MW, COOPERBLACKETER D, MARSHALL VJ, IRIZARRY M et al.: Impaired synaptic plasticity and learning in aged myliod precursor protein transgenic mice. Nat Neurosci, 2:271-76, 1999.

  29. CHURCHLAND PS, SEJNOWSKI TJ: The computational brain. MIT Press, 544 pp. Cambridge, 1992.

  30. DANYSZ W, ZAJACZKOWSKI W, PARSONS CG: Modulation of learning processes by ionotropic glutamate receptors ligands. Behav Pharmacol, 6:455-74, 1995.

  31. DAVIS S, BUTCHER SP, MORRIS RGM: The NMDA receptors antagonists D-2-amino-5-phosphonopentanoate (D-aAP5) impairs spatial- learning and LTP in vivo at intra-cerebral concentrations comparable to those that block LTP in vitro. J Neurosci, 12:21-34, 1992.

  32. DERRICK BE, MARTINEZ JLJ: Associative, bi-directional modifications at the hippocampal mossy fibre-CA3 synapse. Nature, 381:429-34, 1996.

  33. DUDEK SM, Bear MF: Homosynaptic long-term depression and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA, 89:4363-67, 1992.

  34. DUNWIDDIE T, LYNCH G: Long-term potentiation and depression of synaptic responses in the hippocampus: localization and frecuency dependency. J Physiol, 276:353-67, 1978.

  35. ENGERT F, BONHOEFER T: Synapse specificity of long-term potentiation breaks down at short distances. Nature, 388:279-84, 1997.

  36. FISHER SA, DISCHER TM, CAREW TJ: Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci, 20.170-177, 1997.

  37. FITZJOHN SM, BORTOLOTTO ZA, PALMER MJ, DOHERTY AJ, ORNSTEIN PL et al.: The potent mGlu receptor antagonists LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology, 37:1445-58, 1998.

  38. FONTANA DJ, DANIELS SE, WONG EH, CLARK RD, EGLEN RM: The effects of novel selective 5-hydroxytryptamine 5-TH4 receptor ligands in rat spatial navigation. Neuropharmacology, 36:689-96, 1997.

  39. FORTUNE ES, ROSE GJ: Short-term synaptic plasticity contributes to the temporal filtering of electro-sensory information. J Neurosci, 20:7122-7130, 2000.

  40. FORTUNE ES, ROSE GJ: Frecuency-dependent PSP depression contributes to lowpass temporal filtering in Eigenmannia. J Neurosci, 19:7629-7639, 1999.

  41. FREY U, MORRIS RGM: Synaptic tagging and longterm potentiation. Nature, 385:533-36, 1997.

  42. FREY U, MORRIS RGM: Weak before strong: dissociating synaptic-tagging and plasticity-factor accounts of late- LTP. Neuropharmacology, 37:545-52, 1998a.

  43. FREY U, MORRIS RGM: Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci, 21:181-88, 1998b.

  44. FUJII S, SAITO K, MIYAKAWA H, ITO K, KATO H: Reversal of long-term potentiation (depontentiation) induced by tetanus stimulation of the inputs to CA1 neurons of guinea pig hippocampal slices. Brain Res, 555:112-22, 1991.

  45. GOELET P, CASTELLUCCI VF, SCHACHER S, KANDEL ER: The long and the short of long-term memory –a molecular framework. Nature, 322:419-22, 1986.

  46. GRILLNER S, EKEBERG EL, MANIRA A, LANSNER A, PARKER D: Instrisic funtion of a neural network – a vertebrate central pattern generator. Brain Res Rev, 26:184-97, 1998.

  47. HAAG J, BORST A: Amplification of high-frequency synaptic inputs by active dendritic membrane processes. Nature, 379:639-641, 1996.

  48. HARRIS KM: How multiple-synapses boutons could preserve inputs specificity during an interneuronal spread of LTP. TINS, 18(8):365-369, 1995.

  49. HASSELMO ME, SCHNELL E, BARkai E: Dynamics of leaning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci, 15(7 pt. 2): 5249-62, 1995.

  50. HAWKINS RD, KANDEL ER: Is there a cell-biological alphabet for simple forms of learning? Psychol Rev, 91:375-91, 1984.

  51. HAWKINS RD, SON H, ARACIO O: Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res, 118:155-72, 1998b.

  52. HEYNEN AJ, ABRAHAM WC, BEAR MF: Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature, 381:163-66, 1996.

  53. HOH T, BEIKO J, BOON F, WEISS S, CAIN DP: Complex behavioral strategy and reversal learning the water maze without NMDA receptor dependent longterm potentiation. J Neurosci, 19:1-5, 1999.

  54. HÖLSCHER C, MCGLINCHEY L, ANWYL R, ROWAN MJ: 7-Nitro indazole a selective neuronal nitric oxide synthase inhibitor in vivo, impairs spatial learning in the rat. Learn Mem, 2:267-78, 1996.

  55. HOLSCHER C, ANWYL R, ROWAN MJ: Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci, 17:6470-77, 1997.

  56. HSIAO K, CHAPMAN P, NILSEN S, ECKMAN C, HARIGAYA Y et al.: Correlative memory deficit, Ab elevation, and amyloid plaques in transgenic mice. Science, 274:99-102, 1996.

  57. HUERTA PT, LISMAN JE: Bi-directional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron, 15:1053-63, 1995.

  58. HUERTA PT, LISMAN JE: Low-frecuency stimulation at the troughs of theta-oscillation induces long-term depression of previous potentiated CA1 synapses. J Neurophysiol, 75:877-84, 1996.

  59. ISAAC JT, NICOLL RA, MALENKA RC: Evidence for silent synapses: implications for the expression of LTP. Neuron, 15:427-34, 1995.

  60. JEFFERY KJ, MORRIS RGM: Cumulative long-term potentiation in the rat dentate gyrus correlates with, but does not modify, performance in the water maze. Hippocampus, 3:133-40, 1993.

  61. JEFFERY KJ: LTP and spatial learning-where to next? Hippocampus, 7:95-110, 1997.

  62. JONES MV, WESTBROOK GL: The impact of receptor desensitization in fast synaptic transmission. Trends Neurosci, 19:96-101, 1996.

  63. KANDEL ER, SCHWARTZ JH: Molecular biology of learning: modulation of transmitter release. Science, 218:433-43,1982.

  64. KEITH JR, RUDY JW: Why NMDA-receptor-dependent long-term potentiation may not be a mechanisms of learning and memory: reappraisal of the NMDA-receptor bockade strategy. Psychobiology, 18:251-57, 1990.

  65. KENDRICK KM, GUEVARA-GUZMAN R, ZORRILLA J, HILTON MR, BROAD KD et al.: Formation of olfactory memories mediated by nitric oxide. Nature, 388:670-74, 1997.

  66. KENTROS C, HARGREAVES E, HAWKINS RD, KANDEL ER, SHAPIRO M, MULLER RV: Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science, 280:2121-26, 1998.

  67. KIM JJ, YOON KS: Stress: metaplastic effects in the hippocampus. Trends Neurosci, 21:505-509, 1998

  68. KIRKWOOD A, BEAR MF: Homosynaptic long-term depression in the visual cortex. J Neurosci, 14:3404- 12, 1994.

  69. KOEK W, WOODS JH, WINGER GD: MK-801, a proposed noncompetitive antagonits of excitatory aminoacid neurotransmission, produces phencyclidine- like behavioral effects in pigons, rats and Rhesus monkeys. J Pharmacol Exp Ther, 245:969-74, 1988.

  70. KOROL DL, ABEL TW, CHURCH LT, BARNES CA, MCNAUGHTON BL: Hippocampal synaptic enhancement and spatial learning in the Morris swim task. Hippocampus, 3:127-32, 1993.

  71. KULLMANN DM: Amplitude fluctuations of dualcomponent EPSCs in the hippocampal pyramidal cells: implications for long-term potentiation. Neuron, 12:1111-20, 1994.

  72. LADERER R, RADEKE E, MONDADORI C: Facilitation of social learning by treatment with an NMDA receptor antagonist. Behav Neural Biol, 60:220-24, 1993.

  73. LARSON J, WONG D, LYNCH G: Patterned stimulation at the theta frecuency is optimal for the induction of hippocampal long-term potentiation. Brain Res, 368:347-50, 1986.

  74. LEFF P, ROMO H, CALVA JC, ACEVEDO R, GUTIERREZ R, ANTON B: Synaptic plasticity: Understanding the neurobiological mechanisms of learning and memory. Part II. Salud Mental, 24(3):35-44, 2001.

  75. LETTY S, CHILD R, DUMUIS A, PANTALONI A, BOCKAERT J, RONDOUIN G: 5-HT4 receptors impove social olfactory memory in the rat. Neuropharmacology, 36:681-87, 1997.

  76. LEVY WB, STEWARD O: Synapses as associative memory elements in the hippocampal formation. Brain Res, 175:233-45, 1979.

  77. LI H, WEISS SRB, CHUANG D-M, POST RM, ROGAWSKI MA: Bi-directional synaptic plasticity in the rat basolateral amygdala: characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptors antagonists 2Salpha-ethylglutamic acid. J Neurosci, 18:1662-70, 1998

  78. LIAO D, HASELER NA, NALINOW R: Activation of post-synaptically silent synapses during pairedinduced LTP in CA1 region of hippocampal slice. Nature, 375:400-4, 1995.

  79. LIPP HP, WILFER DP: Genetically modified mice and cognition. Curr Opin Neurobiol, 8:272-80, 1998.

  80. LYNCH GS, DUNWIDDIE T, GRIBKOFF V: Heterosynaptic depression: a postsynaptic correlate of longterm potentiation. Nature, 266:737-39, 1977.

  81. LYNCH GS, BAUDRY M: The biochemistry of memory: a new and specific hypothesis. Science, 224:1057-63, 1984.

  82. LYNCH GS: Memory and the brain: unexpected chemistries and a new pharmacology. Neurobiol, Learn, Mem, 70:82-100, 1998.

  83. MALENKA RC: Postsynaptic factors control the duration of synaptic enhancements in area CA1 of the hippocampus. Neuron, 6:53-60, 1991.

  84. MARKRAM H, LUBKE J, FROTSCHER M, SAKMANN B: Regulation of synaptic efficacy by coincidence o postsynaptic APs and EPSPs. Science, 275:213-15, 1997.

  85. MARTIN SJ, GRIMWOOD PD, MORRIS GM: Synaptic plasticity and memory: An evaluation of the hypothesis. Ann Rev Neurosci, 23:649-711, 2000.

  86. MATSUBARA J, HEILIGENBERG W: How well do electric fish electrolocate under jamming? J Comp Physiol, 125:285-290, 1978.

  87. MAYFORD M, WANG J, KANDEL ER, O’DELL TJ: CaMKII regulates the frecuency-response funtion of hippocampal synapses for the production of both LTD and LTP. Cell, 81:891-904, 1995.

  88. MAYFORD M, BACH ME, HUANG Y-Y, WANG L, HAWKINS R, KANDEL ER: Control of memory formation through regulated expression of a CaMKII transgene. Science, 274:1678-83, 1996.

  89. MCEACHERN JC, SHAW CA: An alternative to the LTP orthodoxy: a plasticity-pathology continum model. Brain Res Rev, 22:51-92, 1996.

  90. MCNAUGHTON BL: Activity-dependent modulation of hippocampal synaptic efficacy: some implications for memory processes. In: Neurobiology of the Hippocampus, Siefert W (ed.). pp. 233-52, Academic, London, 1983.

  91. MCNAUGHTON BL, BARNES CA, RAO G, BALDWIN J, RASMUSSEN M: Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci, 6:563-71, 1986.

  92. MONDADORI C, WEISKRANTZ L, BUERKI H, PETSCHKE F, FAGG GE: NMDA receptor antagonists can enhance or impair learning performance in animals. Exp Brain Res, 75:449-56, 1989.

  93. MORRIS RG, ANDERSON E, LYNCH GS, BAUDRY M: Selective impairment of learning and blockade of longterm potentiation by N-methyl-D-aspartate receptor antagonists, AP5. Nature, 319:774-76, 1986.

  94. MORRIS RG: Synaptic plasticity and learning: selective impairment in learning in rats and blockade of longterm potentiation by an N-methyl-D-aspartate receptor antagonists, AP5. J Neurosci, 9:3040-57, 1989.

  95. MORRIS RG, HALLIWELL RF, BOWERY N: Synaptic plasticity and learning II: Do different kinds of plasticity underlie different kinds of learning? Neuropsychologia, 27(1):41-59, 1989 (b).

  96. MORRIS RG, DAVIS S, BUTCHER SP: Hippocampal synaptic plasticity and NMDA receptors: a role in information storage? Philos Trans R Soc, 329:187-204, 1990.

  97. MORRIS RG, FREY U: Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc, 329:187-204, 1997.

  98. MOSER EI, KROBERT KA, MOSER MB, MORRIS RG: Impaired spatial learning after saturation of long-term potentiation. Science, 281:2038-42,1998.

  99. MOSER E, MOSER M-B: Is learning blocked by saturation of synaptic weights in the hippocampus? Neurosci Biobehav Rev, 23:661-72, 1999.

  100. MUMBY DG, WEISAND MP, BARELA PB, SUTHERLAND RJ: LTP saturation contralateral to a hippocampus lesion impairs place learning in rats. Soc Neurosci Abstr, 19:437, 1993.

  101. NGUYEN PV, ABEL T, KANDEL ER: Requirement for a critical period of transcription for induction of late phase of LTP. Science, 265:1104-7, 1994.

  102. NIELSEN KS, MACPHAIL EM, RIEDEL G: Class I mGlu receptor antagonists 1-aminoindan-1, 5-dicarboxylic acid blocks contextual but not cue conditioning in rats. Eur J Pharmacol, 36:105-8, 1997.

  103. ODA Y, KAWASAKI K, MORITA M, KORN H, MITUI H: Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behavior. Nature, 394:182-85, 1998.

  104. OTIS T et al.: Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci, 16:7496-7504, 1996.

  105. PARSONS CG, DANYSZ W, QUACK G: Memantine is a clinically well-tolerated N-methyl-D-aspartate (NMDA) receptor antagonists – review of preclinical data. Neuropharmacology, 38:735-67,1999.

  106. PAVLIDES C, GRENSTEIN YJ, GRUDMAN M, WINSON J: Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of the theta rhythm. Brain Res, 439:383-87, 1988.

  107. PETERSEN CC, MALENKA RC, NICOLL RA, HOPFIELD JJ: All-or-none potentiation at CA3-CA1 synapses. Proc Natl Acad Sci USA, 95:4732-37, 1998.

  108. PIKE FG, MEREDITH RM, OLDING AWA, PAULSEN O: Postsynaptic bursting is essential for ‘Hebbian’ induction of LTP at excitatory synapses in rat hippocampus. J Physiol, 518(pt. 2):571-6, 1999.

  109. RESCOLA RA, WAGNER AR: A theory of Pavlovian conditioning: the effectives of reinforcement and nonreinforcement. In Classical Conditioning. II: Current Research and Theory. Black HL, Prokay WF (eds.). pp. 64-69, Appleton-Century-Crofts, New York, 1972.

  110. RICHTER-LEVIN G, ERRINGTON ML, MAEGARA H, BLISS TVP: Activation of metabotropic glutamate receptors is necessary for long-term potentiation in the dentate gyrus and spatial learning: Neuropharmacology, 33:853-57, 1994.

  111. RIEDEL G, WETZEL W, REYMANN KG: (R,S)-aMethyl- 4-carboxyphentylglycine (MCPG) blocks spatial learning in rats and long-term potentiation in the dentate gyrus in vivo. Neurosci Lett, 167:141-44, 1994.

  112. RIEDEL G, CASABONA G, REYMANN KG: Inhibition of long-term potentiation in the dentate gyrus of freely moving rats by the metabotropic glutamate receptor antagonits MCPG. J Neurosci, 15:87-98, 1995.

  113. ROSE RJ, FORTUNE ES: Frecuency dependent PSP depression contributes to low-pass temporal filtering properties in Eigenmannia. J Neurosci, 19:7629-7639, 1999.

  114. SALT TE, EATON SA: Function of non-NMDA receptors and NMDA receptors in synaptic responses to natural somatosensory stimulation in the ventrobasal thalamus. Exp Brain Res, 77:646-52, 1989.

  115. SAUCIER D, CAIN DP: Spatial learning without NMDA receptor dependent long-term potentiation. Nature, 378:186-89, 1995.

  116. SAUCIER D, HARGREAVES EL, BOON F, VANDERWOLF CH, CAIN D: Detailed behavioral analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: nonspatial pretraining eliminates spatial learning deficits. Behav Neurosci, 110:103-16, 1996.

  117. SEABROOK GR, EASTER A, DAWSON GR, BOWERY BJ: Modulation of long-term potentiation in CA1 region of mouse hippocampal brain slice by GABAA receptor benzodiazepine site ligands. Neuropharmacology, 36:823-30, 1997.

  118. SEABROOK GR, ROSAHL TW: Transgenic animals relevant to Alzheimer’s disease. Neuropharmacology, 38:1-77, 1998.

  119. SEIDENBECHER T, BALSCHUN D, REYMANN KG: Drinking after water deprivation prolongs unsaturated LTP in the dentate gyrus of rats. Physiol Behav, 57:1001-4, 1995.

  120. SELIG DK, NICOLL RA, MAlENKA RC: Hippocampal long-term potentiation preserves the fidelity of postsynaptic responses to pre-synaptic bursts. J Neurosci, 19:1236-46, 1999.

  121. SILLITO AM: Inhibitory circuits and orientation selectivity in the visual cortex. In: Models of the Visual Cortex. Rose D, Dobson VG (eds.). pp. 396-407. Wiley, New York, 1985.

  122. SILLITO AM, MURPHY PC, SALT TE, MOODY CI: Dependence of retinogeniculate transmission in cat on NMDA receptors. J Neurophysiol, 63:347-55, 1990.

  123. STAUBLI U, THIBAULT O, DILORENZO M, LYNCH G: Antagonisms of NMDA receptors impairs acquisition but not retention of olfactory memory. Behav Neurosci, 103:54-60, 1989.

  124. STOPFER M, CAREW TJ: Heterosynaptic facilitation of tail sensory neuron synaptic transmission during habituation in tail induced tail and siphon withdrawal reflexes of Aphysia. J Neurosci, 16:4933-4948, 1996.

  125. STEVENS CF: A million dollar question: Does LTP equal memory? Neuron, 20:1-2, 1998.

  126. SUTHERLAND RJ, DRINGENBERG HC, HOESINING JM: Induction of long-term potentiation at perforant path dentate synapses does not affect place learning o memory. Hippocampus, 3:141-47, 1993.

  127. THIELS E, BARRIONUEVO G, BERGER TW: Excitatory stimulation during post-synaptic inhibition induces long-term depression in hippocampus in vivo. J Neurophysiol, 72:3009-16, 1994.

  128. THOMAS MJ, WATANABE AM, MOODY TD, MAKHINSON, O’DELL TJ: Post-synaptic complex spike bursting enables the induction of LTP by theta frecuency synatic stimulation. J Neurosci, 18:7118-26, 1998.

  129. TOMPA P, FRIEDRICH P: Synaptic metaplasticity and the local charge effect in postsynaptic densities. Trends Neurosci, 21:97-102, 1998.

  130. TIEDTKE PI, BISCHOFF C, SCHMIDT WT: MK-801- induced stereotypy and its antagonism by neuroleptic drugs. J Neural Transm, 81:173-82, 1990.

  131. TURSKI L, KLOCKGETHER T, TURSKI WA, SCHWZ M, SONTAG KH: Blockade of excitaty neurotransmission in the globus palidus induces rigidity and akinesia in the rat: implications for excitatory neurotransmission in pathogenesis of Parkinson’s diseases. Brain Res, 512:125-31, 1990.

  132. WILSHAW D, DAYAN P: Optimal plasticity from matrix memories: What goes up must come down. Neural Commun, 2:85-93, 1990.

  133. XU L, ANWYL R, ROWAN MJ: Behavioral stress as a requirement for the induction of long term-depression in the intact hippocampus. Nature, 387:497-500, 1997.

  134. ZUCKER RS: Short-term synaptic plasticity. Ann Rev Neurosci, 12:13-31,1989.

  135. ZUCKER RS: Calcium-and activity-dependent synaptic plasticity. Curr Opin Neurobiol.,9:305-313, 1999.




2020     |     www.medigraphic.com