Functional basis of associative learning and their relationships with long-term potentiation evoked in the involved neural circuits: Lessons from studies in behaving mammals

Neurobiology of Learning and Memory

Volumn 124, Issue , 2015, Pages 3-18

  Gruart, Agnès ^a   Leal Campanario, Rocío ^a   López Ramos, Juan Carlos ^a   Delgado García, José M ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Activity dependent changes in synaptic strength; Classical eyeblink conditioning; Hippocampus; Long term potentiation; Mice; Operant conditioning; Prefrontal cortex; Rabbits

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; TRANSCRIPTION FACTOR;

ANIMAL BEHAVIOR; BRAIN FUNCTION; COGNITION; CORPUS STRIATUM; EVOKED RESPONSE; EYELID REFLEX; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; INSTRUMENTAL CONDITIONING; LONG TERM POTENTIATION; MAMMAL; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NONHUMAN; PREFRONTAL CORTEX; REVIEW; STATE DEPENDENT LEARNING; SYNAPSE; ANIMAL; BRAIN; CONDITIONED REFLEX; CONDITIONING; HIPPOCAMPUS; LEARNING; NERVE CELL; PHYSIOLOGY;

ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; BRAIN; COGNITION; CONDITIONING, CLASSICAL; CONDITIONING, EYELID; CONDITIONING, OPERANT; HIPPOCAMPUS; LONG-TERM POTENTIATION; NEURONS; PREFRONTAL CORTEX; SYNAPSES;

EID: 84941184328     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.04.006     Document Type: Review

References (89)

1. Amaral D.G. Emerging principles of intrinsic hippocampal organization. Current Opinion in Neurobiology 1993, 3:225-229.
2. Bangasser D.A., Shors T.J. The hippocampus is necessary for enhancements and decrements in learning after a stressful experience. Nature Neuroscience 2007, 10:1401-1403.
3. Barnes C.A., Jung M.W., McNaughton B.L., Korol D.L., Andreasson K., Worley P.F. LTP saturation and spatial learning disruption: Effects of task variables and saturation levels. Journal of Neuroscience 1994, 14:5793-5806.
4. Bartesaghi R., Migliore M., Gessi T. Input-output relations in the entorhinal cortex-dentate-hippocampal system: Evidence for a non-linear transfer of signals. Neuroscience 2006, 142:247-265.
5. Basso M.A., Evinger C. An explanation for reflex blink hyperexcitability in Parkinson's disease. II. Nucleus raphe magnus. The Journal of Neuroscience 1996, 16:7318-7330.
6. Basso M.A., Powers A.S., Evinger C. An explanation for reflex blink hyperexcitability in Parkinson's disease. I. Superior colliculus. The Journal of Neuroscience 1996, 16:7308-7317.
7. Batschelet E. Circular statistics in biology 1981, Academic Press, New York.
8. Benjamin R.M., Jackson J.C., Golden G.T. Cortical projections of the thalamic mediodorsal nucleus in the rabbit. Brain Research 1978, 141:251-265.
9. Berger T.W., Rinaldi P., Weisz D.J., Thompson R.F. Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. Journal of Neurophysiology 1983, 50:1197-1219.
10. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
11. Bliss T.V., Collingridge G.L., Laroche S. Neuroscience. ZAP and ZIP, a story to forget. Science 2006, 313:1058-1059.
12. Bliss T.V.P., Gardner-Medwin A.R. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. The Journal of Physiology (London) 1973, 232:357-374.
13. Bliss T.V.P., Lømo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. The Journal of Physiology (London) 1973, 232:331-356.
14. Buchanan S.L., Thompson R.H., Maxwell B.L., Powell D.A. Efferent connections of the medial prefrontal cortex in the rabbit. Experimental Brain Research 1994, 100:469-483.
15. Carretero-Guillén, A., Pacheco-Calderón, R., Delgado-García, J. M., & Gruart, A. (2013). Involvement of hippocampal inputs and intrinsic circuit in the acquisition of context and cues during classical conditioning in behaving rabbits. Cerebral Cortex (in press). doi:10.1093/cercor/bht321.
16. Clarke J.R., Cammarota M., Gruart A., Izquierdo I., Delgado-García J.M. Plastic modifications induced by object recognition memory processing. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:2652-2657.
17. Collingridge G.L., Kehl S.J., McLennan H. The antagonism of amino acid-induced excitations of rat hippocampal CA1 neurones in vitro. The Journal of Physiology (London) 1983, 334:19-31.
18. Collingridge G.L., Kehl S.J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. The Journal of Physiology (London) 1983, 334:33-46.
19. Cooke S.F., Bear M.F. Stimulus-selective response plasticity in the visual cortex: an assay for the assessment of pathophysiology and treatment of cognitive impairment associated with psychiatric disorders. Biological Psychiatry 2012, 71:487-495.
20. Cutando L., Busquets-Garcia A., Puighermanal E., Gomis-González M., Delgado-García J.M., Gruart A., Maldonado R., Ozaita A. Microglial activation underlies cerebellar deficits produced by repeated cannabis exposure. The Journal of Clinical Investigation 2013, 123:2816-2831.
21. Delgado-García J.M., Gruart A. The role of interpositus nucleus in eyelid conditioned responses. Cerebellum 2002, 1:289-308.
22. Dragoi G., Harris K.D., Buzsáki G. Place representation within hippocampal networks is modified by long-term potentiation. Neuron 2003, 39:843-853.
23. Duran J., Saez I., Gruart A., Guinovart J.J., Delgado-García J.M. Impairment in long-term memory formation and learning-dependent synaptic plasticity in mice lacking glycogen synthase in the brain. Journal of Cerebral Blood Flow and Metabolism 2013, 33:550-556.
24. Eichenbaum H. Conscious awareness, memory and the hippocampus. Nature Neuroscience 1999, 2:775-776.
25. Eleore L., López-Ramos J.C., Guerra-Narbona R., Delgado-García J.M. Role of reuniens nucleus projections to the medial prefrontal cortex and to the hippocampal pyramidal CA1 area in associative learning. PLoS ONE 2011, 6(8):e23538. 10.1371/journal.pone.0023538.
26. Eleore L., López-Ramos J.C., Yi P.J., Delgado-García J.M. The cognitive enhancer T-588 partially compensates the motor associative learning impairments induced by scopolamine injection in mice. Behavioral Neuroscience 2007, 121:1203-1214.
27. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
28. Fontinha B., Delgado-García J.M., Madroñal N., Ribeiro J., Sebastião A.M., Gruart A. Adenosine A2A receptor modulation of hippocampal CA3-CA1 synapse plasticity during associative learning in behaving mice. Neuropsychopharmacology 2009, 34:1865-1874.
29. Fuster J.M. The prefrontal cortex 2008, Academic Press, London.
30. Gil-Sanz C., Delgado-García J.M., Fairén A., Gruart A. Involvement of the mGluR1 receptor in hippocampal synaptic plasticity and associative learning in behaving mice. Cerebral Cortex 2008, 18:1653-1663.
31. Gruart A., Benito E., Delgado-García J.M., Barco A. Enhanced cAMP response element-binding protein activity increases neuronal excitability, hippocampal long-term potentiation, and classical eyeblink conditioning in alert behaving mice. Journal of Neuroscience 2012, 32:17431-17441.
32. Gruart, A., Sánchez-Campusano, R., Fernández-Guizán, A., & Delgado-García, J. M. (2014). A differential and timed contribution of identified hippocampal synapses to associative learning in mice. Cerebral Cortex (in press) . doi:10.1093/cercor/bhu054.
33. Gruart A., Madroñal M., Jurado-Parras M.T., Delgado-García J.M. Synaptic plasticity studies and their applicability in mouse models of neurodegenerative diseases. Translational Neuroscience 2013, 4:134-143.
34. Gruart A., Muñoz M.D., Delgado-Garcia J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. Journal of Neuroscience 2006, 26:1077-1087.
35. Gruart A., Sciarreta C., Valenzuela-Harrington M., Delgado-García J.M., Minichiello L. Mutation at the TrkB PLC-docking site affects hippocampal LTP and associative learning in conscious mice. Learning and Memory 2007, 14:54-62.
36. Harris E.W., Ganong A.H., Cotman C.W. Long-term potentiation in the hippocampus involves activation of N-methyl-d-aspartate receptors. Brain Research 1984, 323:132-137.
37. Hebb D.O. The organization of behavior 1949, Wiley, New York.
38. Heynen A.J., Abraham W.C., Bear M.F. Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 1996, 381:163-166.
39. Jurado-Parras M.T., Gruart A., Delgado-García J.M. Observational learning in mice can be prevented by medial prefrontal cortex stimulation and enhanced by nucleus accumbens stimulation. Learning and Memory 2012, 19:99-106.
40. Jurado-Parras M.T., Sánchez-Campusano R., Castellanos N.P., del-Pozo F., Gruart A., Delgado-García J.M. Differential contribution of hippocampal circuits to appetitive and consummatory behaviors during operant conditioning of behaving mice. Journal of Neuroscience 2013, 33:2293-2304.
41. Kandel E.R. The molecular biology of memory storage: A dialogue between genes and synapses. Science 2001, 294:1030-1038.
42. Kishimoto Y., Kawahara S., Mori H., Mishima M., Kirino Y. Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit ε1. European Journal of Neuroscience 2001, 13:1221-1227.
43. Konorski J. Conditioned reflexes and neuron organization 1948, Cambridge University Press, Cambridge, MA.
44. Kronforst-Collins M.A., Disterhoft J.F. Lesions of the caudal area of rabbit medial prefrontal cortex impair trace eyeblink conditioning. Neurobiology of Learning and Memory 1998, 69:147-162.
45. Leal-Campanario R., Delgado-García J.M., Gruart A. The rostral medial prefrontal cortex regulates the expression of conditioned eyelid responses in behaving rabbits. Journal of Neuroscience 2013, 33:4378-4386.
46. Leal-Campanario R., Fairén A., Delgado-García J.M., Gruart A. Electrical stimulation of the rostral medial prefrontal cortex in rabbits inhibits the expression of conditioned eyelid responses but not their acquisition. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11459-11464.
47. López-Ramos J.C., Guerra-Narbona R., Delgado-García J.M. Different forms of decision-making involve changes in the synaptic strength of the thalamic, hippocampal, and amygdalar afferents to the medial prefrontal cortex. Frontiers in Behavioral Neuroscience 2015, 9(7):1-13. 10.3389/fnbeh.2015.00007.
48. Lucas D., Delgado-García J.M., Escudero B., Albo C., Aza A., Acín-Pérez R., Torres Y., Moreno P., Enríquez J.A., Samper E., Blanco L., Fairén A., Bernad A., Gruart A. Increased learning and brain long-term potentiation in aged mice lacking DNA polymerase μ. PLoS ONE 2013, 8(1):e53243. 10.1371/journal.pone.0053243.
49. Lynch M.A. Long-term potentiation and memory. Physiological Reviews 2004, 84:87-136.
50. Madroñal N., Delgado-García J.M., Gruart A. Differential effects of long-term potentiation evoked at the CA3 CA1 synapse before, during, and after the acquisition of classical eyeblink conditioning in behaving mice. Journal of Neuroscience 2007, 27:12139-12146.
51. Madroñal N., Gruart A., Delgado-García J.M. Differing presynaptic contributions to LTP and associative learning in behaving mice. Frontiers in Behavioral Neuroscience 2009, 3:7. 10.3389/neuro.08.007.2009.
52. Madroñal N., Gruart A., Sacktor T.C., Delgado-García J.M. PKM inhibition reverses learning-induced increases in hippocampal synaptic strength and memory during trace eyeblink conditioning. PLoS ONE 2010, 5(4):e10400. 10.1371/journal.pone.0010400.
53. Madroñal N., Gruart A., Valverde O., Espadas I., Moratalla R., Delgado-García J.M. Involvement of cannabinoid CB1 receptor in associative learning and in hippocampal CA3-CA1 synaptic plasticity. Cerebral Cortex 2012, 22:550-566.
54. Malenka R., Nicoll R.A. Long-term potentiation-A decade of progress?. Science 1999, 285:1870-1874.
55. Mardia K.V., Jupp P.E. Directional statistics 1999, Wiley, Chichester.
56. Marr D. Simple memory: a theory of archicortex. Philosophical Transactions of the Royal Society B: Biological Sciences 1971, 262:23-81.
57. McEchron M.D., Disterhoft J.F. Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. Journal of Neurophysiology 1997, 78:1030-1044.
58. McEchron M.D., Tseng W., Disterhoft J.F. Single neurons in CA1 hippocampus encode trace interval duration during trace heart rate (fear) conditioning in rabbit. Journal of Neuroscience 2003, 23:1535-1547.
59. McHugh T.J., Jones M.W., Quinn J.J., Balthasar N., Coppari R., Elmquist J.K., Lowell B.B., Fanselow M.S., Wilson M.A., Tonegawa S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 2007, 317:94-99.
60. McNaughton B.L., Douglas R.M., Goddard G.V. Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Research 1978, 157:277-293.
61. Mokin M., Keifer J. Expression of the immediate-early gene-encoded protein Egr-1 (zif268) during in vitro classical conditioning. Learning and Memory 2005, 12:144-149.
62. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annual Review of Neuroscience 2008, 31:69-89.
63. Moyer J.R., Deyo R.A., Disterhoft J.F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience 1990, 104:243-252.
64. Múnera A., Gruart A., Muñoz M.D., Fernández-Mas R., Delgado-García J.M. Discharge properties of identified CA1 and CA3 hippocampus neurons during unconditioned and conditioned eyelid responses in cats. Journal of Neurophysiology 2001, 86:2571-2582.
65. Nakashiba T., Young J.Z., McHugh T.J., Buhl D.L., Tonegawa S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319:1260-1264.
66. Narayanan N.S., Land B.B., Solder J.E., Deisseroth K., DiLeone R.J. Prefrontal D1 dopamine signaling is required for temporal control. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:20726-20731.
67. Neves G., Cooke S.F., Bliss T.V. Synaptic plasticity, memory and the hippocampus: A neural network approach to causality. Nature Reviews Neuroscience 2008, 9:65-75.
68. -/- mice and in hippocampal siRNA silenced Drd1a mice. Journal of Neuroscience 2010, 30:12288-12300.
69. Pujadas L., Gruart A., Delgado L., Teixeira C.M., Rossi d., de Lecea L., Martínez A., Delgado-García J.M., Soriano E. Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. Journal of Neuroscience 2010, 30:4636-4649.
70. Ramirez S., Liu X., Lin P.A., Suh J., Pignatelli M., Redondo R.L., Ryan T.J., Tonegawa S. Creating a false memory in the hippocampus. Science 2013, 341:387-391.
71. Ray J.P., Russchen F.T., Fuller T.A., Price J.L. Sources of presumptive glutamatergic/aspartatergic afferents to the mediodorsal nucleus of the thalamus in the rat. Journal of Comparative Neurology 1992, 320:435-456.
72. Redondo R.L., Kim J., Arons A.L., Ramirez S., Liu X., Tonegawa S. Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 2014, 513:426-430.
73. Rescorla R.A. Behavioral studies of Pavlovian conditioning. Annual Review of Neuroscience 1988, 11:329-352.
74. Sahún I., Delgado-García J.M., Amador-Arjona A., Giralt A., Alberch J., Dierssen M., Gruart A. Dissociation between CA3-CA1 synaptic plasticity and associative learning in TgNTRK3 transgenic mice. Journal of Neuroscience 2007, 27:2253-2260.
75. Sánchez-Campusano R., Gruart A., Delgado-García J.M. Timing and causality in the generation of learned eyelid responses. Frontiers in Integrative Neuroscience 2011, 5:39. 10.3389/fnint.2011.00039.
76. Sanders M.J., Fanselow M.S. Pre-training prevents context fear conditioning deficits produced by hippocampal NMDA receptor blockade. Neurobiology of Learning and Memory 2003, 80:123-129.
77. Segal M., Disterhoft J.F., Olds J. Hippocampal unit activity during classical aversive and appetitive conditioning. Science 1972, 175:792-794.
78. Segal M., Olds J. Behavior of units in hippocampal circuit of the rat during learning. Journal of Neurophysiology 1972, 35:680-690.
79. Servatius R.J., Shors T.J. Early acquisition, but not retention, of classically conditioned eyeblink responses is N-methyl-d-aspartate (NMDA) receptor dependent. Behavioral Neuroscience 1996, 110:1040-1048.
80. Shipton O.A., El-Gaby M., Apergis-Schoute J., Deisseroth K., Bannerman D.M., Paulsen O., Kohl M.M. Left-right dissociation of hippocampal memory processes in mice. Proceedings of the National academy of Sciences of the United States of America 2014, 111:15238-15243.
81. Stan Leung L., Shen B. Hippocampal CA1 kindling but not long-term potentiation disrupts spatial memory performance. Learning and Memory 2006, 13:18-26.
82. Thompson R.F. The neural basis of basic associative learning of discrete behavioral responses. Trends in Neurosciences 1988, 11:152-155.
83. Thomson A.M. Facilitation, augmentation and potentiation at central synapses. Trends in Neurosciences 2000, 23:305-312.
84. Vega-Flores G., Rubio S.E., Jurado-Parras M.T., Gómez-Climent M.A., Hampe C.S., Manto M., Soriano E., Pascual M., Gruart A., Delgado-García J.M. The GABAergic septohippocampal pathway is directly involved in internal processes related to operant reward learning. Cerebral Cortex 2014, 24:2093-2107.
85. Wang S.H., Morris R.G. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annual Review of Psychology 2010, 61:49-79.
86. Weiss C., Sametsky E., Sasse A., Spiess J., Disterhoft J.F. The hippocampus is necessary for enhancements and impairments of learning following stress. Learning and Memory 2005, 12:138-143.
87. Weisz D.J., Clark G.A., Thompson R.F. Increased responsivity of dentate granule cells during nictitating membrane response conditioning in rabbit. Behavioural Brain Research 1984, 12:145-154.
88. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
89. Zucker R.S., Regehr W.G. Short term synaptic plasticity. Annual Review of Physiology 2002, 64:355-405.