Bridging the interval: Theory and neurobiology of trace conditioning

Behavioural Processes

Volumn 101, Issue , 2014, Pages 103-111

  Raybuck, Jonathan D ^a   Lattal, K Matthew ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Amygdala; Consolidation; Fear; Hippocampus; Learning theory; Memory; Neurobiology

Indexed keywords

AMYGDALA; CONSOLIDATION; FEAR; HIPPOCAMPUS; LEARNING THEORY; MEMORY; NEUROBIOLOGY;

ANIMALS; ASSOCIATION LEARNING; BRAIN; CONDITIONING, CLASSICAL; FEAR; PSYCHOLOGICAL THEORY;

EID: 84894232849     PISSN: 03766357     EISSN: 18728308     Source Type: Journal    
DOI: 10.1016/j.beproc.2013.08.016     Document Type: Review

References (134)

1. Balsam P. Relative time in trace conditioning. Annals of the New York Academy of Sciences 1984, 423:211-227.
2. Balsam P.D., Drew M.R., Yang C. Timing at the start of associative learning. Learning & Motivation 2002, 33(1):141-155.
3. Bang S.J., Brown T.H. Muscarinic receptors in perirhinal cortex control trace conditioning. Journal of Neuroscience 2009, 29:4346-4350.
4. Bangasser D.A., Waxler D.E., Santollo J., Shors T.J. Trace conditioning and the hippocampus: the importance of contiguity. Journal of Neuroscience 2006, 26:8702-8706.
5. Bannerman D.M., Grubb M., Deacon R.M.J., Yee B.K., Feldon J., Rawlins J.N.P. Ventral hippocampal lesions affect anxiety but not spatial learning. Behavioural Brain Research 2003, 139:197-213.
6. Bannerman D.M., Rawlins J.N.P., McHugh S.B., Deacon R.M.J., Yee B.K., Bast T., Zhang W., Pothuizen H.H.J., Feldon J. Regional dissociations within the hippocampus - memory and anxiety. Neuroscience and Biobehavioral Reviews 2004, 28:273-283.
7. Barbey A.K., Koenigs M., Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex 2013, 49:1195-1205.
8. Barnet R.C., Hunt P.S. Trace and long-delay fear conditioning in the developing rat. Learning & Behavior 2005, 33:437-443.
9. Baysinger A.N., Kent B.A., Brown T.H. Muscarinic receptors in amygdala control trace fear conditioning. PLoS ONE 2012, 7:e45720.
10. Beeman C.L., Bauer P.S., Pierson J.L., Quinn J.J. Hippocampus and medial prefrontal cortex contributions to trace and contextual fear memory expression over time. Learning & Memory 2013, 20:336-343.
11. Bevins R.A., Ayres J.J.B. One-trial context fear conditioning as a function of the interstimulus interval. Animal Learning & Behavior 1995, 23:400-410.
12. Bolles R.C., Collier A.C., Bouton M.E., Marline N.A. Some tricks for ameliorating the trace-conditioning deficit. Bulletin of the Psychonomic Society 1978, 11:403-406.
13. Brzózka M.M., Rossner M.J. Deficits in trace fear memory in a mouse model of the schizophrenia risk gene TCF4. Behavioural Brain Research 2013, 237:348-356.
14. Burman M.A., Gewirtz J.C. Timing of fear expression in trace and delay conditioning measured by fear-potentiated startle in rats. Learning & Memory 2004, 11:205-212.
15. Burman M.A., Starr M.J., Gewirtz J.C. Dissociable effects of hippocampus lesions on expression of fear and trace fear conditioning memories in rats. Hippocampus 2006, 16:103-113.
16. Büchel C., Dolan R.J., Armony J.L., Friston K.J. Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. Journal of Neuroscience 1999, 19:10869-10876.
17. Chowdhury N., Quinn J.J., Fanselow M.S. Dorsal hippocampus involvement in trace fear conditioning with long, but not short, trace intervals in mice. Behavioral Neuroscience 2005, 119:1396-1402.
18. Cole R.P., Barnet R.C., Miller R.R. Temporal encoding in trace conditioning. Animal Learning & Behavior 1995, 23:144-153.
19. Cox D., Czerniawski J., Ree F., Otto T. Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning. Neurobiology of Learning and Memory 2013, 10.1016/j.nlm.2013.05.009.
20. Czerniawski J., Ree F., Chia C., Otto T. Dorsal versus ventral hippocampal contributions to trace and contextual conditioning: differential effects of regionally selective NMDA receptor antagonism on acquisition and expression. Hippocampus 2012, 22:1528-1539.
21. Czerniawski J., Yoon T., Otto T. Dissociating space and trace in dorsal and ventral hippocampus. Hippocampus 2009, 19:20-32.
22. Dalley J.W., Cardinal R.N., Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews 2004, 28:771-784.
23. Davis J.A., Gould T.J. beta2 subunit-containing nicotinic receptors mediate the enhancing effect of nicotine on trace cued fear conditioning in C57BL/6 mice. Psychopharmacology 2007, 190:343-352.
24. Davis M., Schlesinger L.S., Sorenson C.A. Temporal specificity of fear conditioning: effects of different conditioned stimulus-unconditioned stimulus intervals on the fear-potentiated startle effect. Journal of Experimental Psychology: Animal Behavior Processes 1989, 15:295-310.
25. Delamater A.R., Holland P.C. The influence of CS-US interval on several different indices of learning in appetitive conditioning. Journal of Experimental Psychology: Animal Behavior Processes 2008, 34:202-222.
26. Descalzi G., Li X., Chen T., Mercaldo V., Koga K., Zhuo M. Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Molecular Brain 2012, 5:6.
27. Desmedt A., Marighetto A., Garcia R., Jaffard R. The effects of ibotenic hippocampal lesions on discriminative fear conditioning to context in mice: impairment or facilitation depending on the associative value of a phasic explicit cue. European Journal of Neuroscience 2003, 17:1953-1963.
28. Drew M.R., Zupan B., Cooke A., Couvillon P.A., Balsam P.D. Temporal control of conditioned responding in goldfish. Journal of Experimental Psychology. Animal Behavior Processes 2005, 31:31-39.
29. Díaz-Mataix L., Ruiz Martinez R.C., Schafe G.E., LeDoux J.E., Doyère V. Detection of a temporal error triggers reconsolidation of amygdala-dependent memories. Current Biology 2013, 23:467-472.
30. Ellison G.D. Differential salivary conditioning to traces. Journal of Comparative and Physiological Psychology 1964, 57:373-380.
31. Esclassan F., Coutureau E., Di Scala G., Marchand A.R. A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning. Journal of Neuroscience 2009, 29:8087-8093.
32. Esclassan F., Coutureau E., Di Scala G., Marchand A.R. Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 2009, 19:33-44.
33. Fanselow M.S., Dong H. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
34. Fanselow M.S., Gale G.D. The amygdala, fear, and memory. Annals of the New York Academy of Sciences 2003, 985:125-134.
35. Fanselow M.S., LeDoux J.E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999, 23:229-232.
36. Fanselow M.S., Poulos A.M. The neuroscience of mammalian associative learning. Annual Review of Psychology 2005, 56:207-234.
37. Fendt M., Fanselow M.S., Koch M. Lesions of the dorsal hippocampus block trace fear conditioned potentiation of startle. Behavioral Neuroscience 2005, 119:834-838.
38. Flesher M.M., Butt A.E., Kinney-Hurd B.L. Differential acetylcholine release in the prefrontal cortex and hippocampus during pavlovian trace and delay conditioning. Neurobiology of Learning and Memory 2011, 96:181-191.
39. Gilmartin M.R., Helmstetter F.J. Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex. Learning & Memory 2010, 17:289-296.
40. Gilmartin M.R., McEchron M.D. Single neurons in the dentate gyrus and CA1 of the hippocampus exhibit inverse patterns of encoding during trace fear conditioning. Behavioral Neuroscience 2005, 119:164-179.
41. Gilmartin M.R., McEchron M.D. Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning. Behavioral Neuroscience 2005, 119:1496-1510.
42. Gilmartin M.R., Kwapis J.L., Helmstetter F.J. Trace and contextual fear conditioning are impaired following unilateral microinjection of muscimol in the ventral hippocampus or amygdala, but not the medial prefrontal cortex. Neurobiology of Learning and Memory 2012, 97:452-464.
43. Gilmartin M.R., Kwapis J.L., Helmstetter F.J. NR2A- and NR2B-containing NMDA receptors in the prelimbic medial prefrontal cortex differentially mediate trace, delay, and contextual fear conditioning. Learning & Memory 2013, 20:290-294.
44. Gilmartin M.R., Miyawaki H., Helmstetter F.J., Diba K. Prefrontal activity links nonoverlapping events in memory. Journal of Neuroscience 2013, 33:10910-10914.
45. Gould T.J., Feiro O., Moore D. Nicotine enhances trace cued fear conditioning but not delay cued fear conditioning in C57BL/6 mice. Behavioural Brain Research 2004, 155:167-173.
46. Guimarãis M., Gregório A., Cruz A., Guyon N., Moita M.A. Time determines the neural circuit underlying associative fear learning. Frontiers in Behavioral Neuroscience 2011, 5:89.
47. Han C.J., O'Tuathaigh C.M., van Trigt L., Quinn J.J., Fanselow M.S., Mongeau R., Koch C., Anderson D.J. Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:13087-13092.
48. Hartley A.A., Speer N.K. Locating and fractionating working memory using functional neuroimaging: storage, maintenance, and executive functions. Microscopy Research and Technique 2000, 51:45-53.
49. Hasselmo M.E., Brandon M.P. Linking cellular mechanisms to behavior: entorhinal persistent spiking and membrane potential oscillations may underlie path integration, grid cell firing, and episodic memory. Neural Plasticity 2008, 2008:658323.
50. Hayashi M.L., Rao B.S.S., Seo J., Choi H., Dolan B.M., Choi S., Chattarji S., Tonegawa S. Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11489-11494.
51. Holmes A., Singewald N. Individual differences in recovery from traumatic fear. Trends in Neurosciences 2013, 36:23-31.
52. Hoover W.B., Vertes R.P. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Structure & Function 2007, 212:149-179.
53. Huang C., Chiang Y., Liang K., Thompson R.F., Liu I.Y. Extra-cellular signal-regulated kinase 1/2 (ERK1/2) activated in the hippocampal CA1 neurons is critical for retrieval of auditory trace fear memory. Brain Research 2010, 1326:143-151.
54. Huerta P.T., Sun L.D., Wilson M.A., Tonegawa S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 2000, 25:473-480.
55. Hunt P.S., Richardson R. Pharmacological dissociation of trace and long-delay fear conditioning in young rats. Neurobiology of Learning and Memory 2007, 87:86-92.
56. Hunt P.S., Barnet R.C., Shea M.E., Baker E.M. Cholinergic modulation of trace conditioning trained in serial compound: a developmental analysis. Neurobiology of Learning and Memory 2006, 86:311-321.
57. Hunt P.S., Levillain M.E., Spector B.M., Kostelnik L.A. Post-training ethanol disrupts trace conditioned fear in rats: effects of timing of ethanol, dose and trace interval duration. Neurobiology of Learning and Memory 2009, 91:73-80.
58. Jansma J.M., Ramsey N.F., Coppola R., Kahn R.S. Specific versus nonspecific brain activity in a parametric N-back task. NeuroImage 2000, 12:688-697.
59. Joscelyne A., Kehoe E.J. Time and stimulus specificity in extinction of the conditioned nictitating membrane response in the rabbit (Oryctolagus cuniculus). Behavioral Neuroscience 2007, 121:50-62.
60. Kaczorowski C.C., Sametsky E., Shah S., Vassar R., Disterhoft J.F. Mechanisms underlying basal and learning-related intrinsic excitability in a mouse model of Alzheimer's disease. Neurobiology of Aging 2011, 32:1452-1465.
61. Kalat J.W., Rozin P. "Learned safety" as a mechanism in long-delay taste-aversion learning in rats. Journal of Comparative and Physiological Psychology 1973, 83:198-207.
62. Kamin L.J. Trace conditioning of the conditioned emotional response. Journal of Comparative and Physiological Psychology 1961, 54:149-153.
63. Kehoe E.J., Joscelyne A. Temporally specific extinction of conditioned responses in the rabbit (Oryctolagus cuniculus) nictitating membrane preparation. Behavioral Neuroscience 2005, 119:1011-1022.
64. Kehoe E.J., Ludvig E.A., Sutton R.S. Magnitude and timing of conditioned responses in delay and trace classical conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus). Behavioral Neuroscience 2009, 123:1095-1101.
65. Kent B.A., Brown T.H. Dual functions of perirhinal cortex in fear conditioning. Hippocampus 2012, 22:2068-2079.
66. Kholodar-Smith D.B., Boguszewski P., Brown T.H. Auditory trace fear conditioning requires perirhinal cortex. Neurobiology of Learning and Memory 2008, 90:537-543.
67. Kim J.J., Jung M.W. Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neuroscience and Biobehavioral Reviews 2006, 30:188-202.
68. Knight D.C., Cheng D.T., Smith C.N., Stein E.A., Helmstetter F.J. Neural substrates mediating human delay and trace fear conditioning. Journal of Neuroscience 2004, 24:218-228.
69. Kwapis J.L., Jarome T.J., Schiff J.C., Helmstetter F.J. Memory consolidation in both trace and delay fear conditioning is disrupted by intra-amygdala infusion of the protein synthesis inhibitor anisomycin. Learning & Memory 2011, 18:728-732.
70. Lattal K.M., Abel T. An immediate-shock freezing deficit with discrete cues: a possible role for unconditioned stimulus processing mechanisms. Journal of Experimental Psychology. Animal Behavior Processes 2001, 27:394-406.
71. Lewis M.C., Gould T.J. Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice. Hippocampus 2007, 17:462-470.
72. Lewis M.C., Gould T.J. Signal transduction mechanisms within the entorhinal cortex that support latent inhibition of cued fear conditioning. Neurobiology of Learning and Memory 2007, 88:359-368.
73. Lockhart R.A. Comments regarding multiple response phenomena in long interstimulus interval conditioning. Psychophysiology 1966, 3:108-114.
74. Mao R., Page D.T., Merzlyak I., Kim C., Tecott L.H., Janak P.H., Rubenstein J.L.R., Sur M. Reduced conditioned fear response in mice that lack Dlx1 and show subtype-specific loss of interneurons. Journal of Neurodevelopmental Disorders 2009, 1:224-236.
75. Maggio N., Segal M. Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. Journal of Neuroscience 2007, 27:5757-5765.
76. Marlin N.A. Contextual associations in trace conditioning. Animal Learning & Behavior 1981, 9(4):519-523.
77. McEchron M.D., Bouwmeester H., Tseng W., Weiss C., Disterhoft J.F. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 1998, 8:638-646.
78. McEchron M.D., Tseng W., Disterhoft J.F. Neurotoxic lesions of the dorsal hippocampus disrupt auditory-cued trace heart rate (fear) conditioning in rabbits. Hippocampus 2000, 10:739-751.
79. McLaughlin J., Skaggs H., Churchwell J., Powell D.A. Medial prefrontal cortex and pavlovian conditioning: trace versus delay conditioning. Behavioral Neuroscience 2002, 116:37-47.
80. Misane I., Tovote P., Meyer M., Spiess J., Ogren S.O., Stiedl O. Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 2005, 15:418-426.
81. Molet M., Miguez G., Cham H.X., Miller R.R. When does integration of independently acquired temporal relationships take place?. Journal of Experimental Psychology. Animal Behavior Processes 2012, 38:369-380.
82. Molet M., Miller R.R. Timing: an attribute of associative learning. Behavioural Processes 2013, 10.1016/j.beproc.2013.05.015.
83. Morales G.J., Ramcharan E.J., Sundararaman N., Morgera S.D., Vertes R.P. Analysis of the actions of nucleus reuniens and the entorhinal cortex on EEG and evoked population behavior of the hippocampus. Conf Proc IEEE Eng Med Biol Soc 2007 2007, 2480-2484.
84. Moscovitch A., LoLordo V.M. Role of safety in the Pavlovian backward fear conditioning procedure. Journal of Comparative and Physiological Psychology 1968, 66:673-678.
85. Moustafa A.A., Wufong E., Servatius R.J., Pang K.C.H., Gluck M.A., Myers C.E. Why trace and delay conditioning are sometimes (but not always) hippocampal dependent: a computational model. Brain Research 2013, 1493:48-67.
86. Moyer J.R.J., Deyo R.A., Disterhoft J.F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience 1990, 104:243-252.
87. Ohno M., Chang L., Tseng W., Oakley H., Citron M., Klein W.L., Vassar R., Disterhoft J.F. Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. European Journal of Neuroscience 2006, 23:251-260.
88. Pape H., Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiological Reviews 2010, 90:419-463.
89. Pavlov I.P. Conditioned Reflexes, An Investigation of the Physiological Activity of the Cerebral Cortex 1927, Oxford University Press, London.
90. Perry J.L., Joseph J.E., Jiang Y., Zimmerman R.S., Kelly T.H., Darna M., Huettl P., Dwoskin L.P., Bardo M.T. Prefrontal cortex and drug abuse vulnerability: translation to prevention and treatment interventions. Brain Research Reviews 2011, 65:124-149.
91. Peters J., Kalivas P.W., Quirk G.J. Extinction circuits for fear and addiction overlap in prefrontal cortex. Learning & Memory 2009, 16:279-288.
92. Peters M., Bletsch M., Catapano R., Zhang X., Tully T., Bourtchouladze R. RNA interference in hippocampus demonstrates opposing roles for CREB and PP1alpha in contextual and temporal long-term memory. Genes, Brain, and Behavior 2009, 8:320-329.
93. Peterson B.S., Skudlarski P., Gatenby J.C., Zhang H., Anderson A.W., Gore J.C. An fMRI study of Stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems. Biological Psychiatry 1999, 45:1237-1258.
94. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 1992, 106:274-285.
95. Quinn J.J., Loya F., Ma Q.D., Fanselow M.S. Dorsal hippocampus NMDA receptors differentially mediate trace and contextual fear conditioning. Hippocampus 2005, 15:665-674.
96. Quinn J.J., Ma Q.D., Tinsley M.R., Koch C., Fanselow M.S. Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learning & Memory 2008, 15:368-372.
97. Quinn J.J., Oommen S.S., Morrison G.E., Fanselow M.S. Post-training excitotoxic lesions of the dorsal hippocampus attenuate forward trace, backward trace, and delay fear conditioning in a temporally specific manner. Hippocampus 2002, 12:495-504.
98. Raybuck J.D., Gould T.J. Nicotine withdrawal-induced deficits in trace fear conditioning in C57BL/6 mice--a role for high-affinity beta2 subunit-containing nicotinic acetylcholine receptors. European Journal of Neuroscience 2009, 29:377-387.
99. Raybuck J.D., Gould T.J. The role of nicotinic acetylcholine receptors in the medial prefrontal cortex and hippocampus in trace fear conditioning. Neurobiology of Learning and Memory 2010, 94:353-363.
100. Raybuck J.D., Lattal K.M. Double dissociation of amygdala and hippocampal contributions to trace and delay fear conditioning. PLoS ONE 2011, 6:e15982.
101. Rescorla R.A. Effect of a stimulus intervening between CS and US in autoshaping. Journal of Experimental Psychology. Animal Behavior Processes 1982, 8:131-141.
102. Rogers J.L., Hunsaker M.R., Kesner R.P. Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiology of Learning and Memory 2006, 86:72-81.
103. Rudy J.W., Huff N.C., Matus-Amat P. Understanding contextual fear conditioning: insights from a two-process model. Neuroscience and Biobehavioral Reviews 2004, 28:675-685.
104. Runyan J.D., Dash P.K. Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiology of Learning and Memory 2004, 82:65-70.
105. Runyan J.D., Dash P.K. Inhibition of hippocampal protein synthesis following recall disrupts expression of episodic-like memory in trace conditioning. Hippocampus 2005, 15:333-339.
106. Runyan J.D., Moore A.N., Dash P.K. A role for prefrontal cortex in memory storage for trace fear conditioning. Journal of Neuroscience 2004, 24:1288-1295.
107. Santini E., Quirk G.J., Porter J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. Journal of Neuroscience 2008, 28:4028-4036.
108. Sarter M., Gehring W.J., Kozak R. More attention must be paid: the neurobiology of attentional effort. Brain Research Reviews 2006, 51:145-160.
109. Selcher J.C., Atkins C.M., Trzaskos J.M., Paylor R., Sweatt J.D. A necessity for MAP kinase activation in mammalian spatial learning. Learning & Memory 1999, 6:478-490.
110. Selden N.R., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42:335-350.
111. Seo D., Pang M., Shin M., Kim H., Choi J. Hippocampal NMDA receptors are necessary for auditory trace fear conditioning measured with conditioned hypoalgesia in rats. Behavioural Brain Research 2008, 192:264-268.
112. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2011, 36:529-538.
113. Smith D.R., Gallagher M., Stanton M.E. Genetic background differences and nonassociative effects in mouse trace fear conditioning. Learning & Memory 2007, 14:597-605.
114. Stafford J.M., Maughan D.K., Ilioi E.C., Lattal K.M. Exposure to a fearful context during periods of memory plasticity impairs extinction via hyperactivation of frontal-amygdalar circuits. Learning & Memory 2013, 20:156-163.
115. Steenland H.W., Li X., Zhuo M. Predicting aversive events and terminating fear in the mouse anterior cingulate cortex during trace fear conditioning. Journal of Neuroscience 2012, 32:1082-1095.
116. Suh J., Rivest A.J., Nakashiba T., Tominaga T., Tonegawa S. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 2011, 334:1415-1420.
117. Tam S.K., Bonardi C. Dorsal hippocampal involvement in appetitive trace conditioning and interval timing. Behavioral Neuroscience 2012, 126:258-269.
118. Thomas G.V., Robertson D., Cunniffe G. Facilitation of responding in a filled-delay trace autoshaping procedure: an occasion-setting hypothesis. Learning & Motivation 1989, 20(3):225-241.
119. Thompson E., Kochli D., Quinn J. Amygdala involvement in context, but not trace, fear conditioning. Society for Neuroscience 2012, 598(12):CCC76.
120. Trivedi M.A., Coover G.D. Lesions of the ventral hippocampus, but not the dorsal hippocampus, impair conditioned fear expression and inhibitory avoidance on the elevated T-maze. Neurobiology of Learning and Memory 2004, 81:172-184.
121. Trivedi M.A., Coover G.D. Neurotoxic lesions of the dorsal and ventral hippocampus impair acquisition and expression of trace-conditioned fear-potentiated startle in rats. Behavioural Brain Research 2006, 168:289-298.
122. Urushihara K., Miller R.R. Backward blocking in first-order conditioning. Journal of Experimental Psychology. Animal Behavior Processes 2010, 36:281-295.
123. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 2004, 51:32-58.
124. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 2006, 142:1-20.
125. Wagner A.F., Hunt P.S. Impaired trace fear conditioning following neonatal ethanol: reversal by choline. Behavioral Neuroscience 2006, 120:482-487.
126. Wang R., Phang R., Hsu P., Wang W., Huang H., Liu I.Y. In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 2013, 10.1002/hipo.22123.
127. Wanisch K., Tang J., Mederer A., Wotjak C.T. Trace fear conditioning depends on NMDA receptor activation and protein synthesis within the dorsal hippocampus of mice. Behavioural Brain Research 2005, 157:63-69.
128. Weitemier A.Z., Ryabinin A.E. Subregion-specific differences in hippocampal activity between delay and trace fear conditioning: an immunohistochemical analysis. Brain Research 2004, 995:55-65.
129. Williams B.A. Marking and bridging versus conditioned reinforcement. Animal Learning and Behavior 1991, 19(3):264-269.
130. Woodruff-Pak D.S., Disterhoft J.F. Where is the trace in trace conditioning?. Trends in Neurosciences 2008, 31:105-112.
131. 2+/calmodulin-dependent protein kinase IV. European Journal of Neuroscience 2008, 27:1923-1932.
132. Yoon T., Otto T. Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning. Neurobiology of Learning and Memory 2007, 87:464-475.
133. Yttri E.A., Burk J.A., Hunt P.S. Intermittent ethanol exposure in adolescent rats: dose-dependent impairments in trace conditioning. Alcoholism, Clinical and Experimental Research 2004, 28:1433-1436.
134. Zhao M., Toyoda H., Ko S.W., Ding H., Wu L., Zhuo M. Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. Journal of Neuroscience 2005, 25:7385-7392.