Balancing the Contributions of Multiple Neural Systems During Learning and Memory

  • Paul E. GoldEmail author


From the research era in the early 1970s that defined Ray Kesner’s and my early forays into memory research, the identification of memory attributes that depend on different neural systems has led to identification of neuroendocrine mechanisms that regulate memory processing across those systems. This chapter examines important points of convergence between investigations into multiple memory systems and memory modulation. Reviewed here is evidence showing that neurotransmitter release and energy availability within these systems participate importantly in regulating neural processing during times of learning and memory. In particular, the findings reveal neurochemical responses across neural systems while rats are engaged in different learning and memory tasks. These results thereby integrate information about the brain systems that participate in processing different attributes of memory with neurochemical regulation of the processing of different attributes of memory across neural systems.


Acetylcholine Glycogen Astrocytes Glia Plasticity Metabolism Striatum Hippocampus Learning Memory 


  1. Abbas, A. K., Dozmorov, M., Li, R., Huang, F. S., Hellberg, F., Danielson, J., Tian, Y., Ekstrom, J., Sandberg, M., & Wigstrom, H. (2009). Persistent LTP without triggered protein synthesis. Neuroscience Research, 63, 59–65.CrossRefPubMedGoogle Scholar
  2. Archer, T., Söderberg, U., Ross, S. B., & Jonsson, G. (1984). Role of olfactory bulbectomy and DSP4 treatment in avoidance learning in the rat. Behavioral Neuroscience, 98, 496–505.CrossRefPubMedGoogle Scholar
  3. Bermudez-Rattoni, F., Introini-Collison, I. B., & McGaugh, J. L. (1991). Reversible inactivation of the insular cortex by tetrodotoxin produces retrograde and anterograde amnesia for inhibitory avoidance and spatial learning. Proceedings of the National Academy of Science USA, 88, 5379–5382.CrossRefGoogle Scholar
  4. Cahill, L., & Alkire, M. T. (2003). Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding. Neurobiology of Learning and Memory, 79, 194–198.CrossRefPubMedGoogle Scholar
  5. Chang, Q., & Gold, P. E. (2003a). Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behavioural Brain Research, 144, 19–24.CrossRefPubMedGoogle Scholar
  6. Chang, Q., & Gold, P. E. (2003b). Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. Journal of Neuroscience, 23, 3001–3005.PubMedGoogle Scholar
  7. Chang, Q., & Gold, P. E. (2004). Inactivation of dorsolateral striatum impairs acquisition of ­response learning in cue-deficient but not cue-available conditions. Behavioral Neuroscience, 118, 383–388.CrossRefPubMedGoogle Scholar
  8. Cherkin, A. (1969). Kinetics of memory consolidation: Role of amnesic treatment parameters. Proceedings of the National Academy of Science USA, 63, 1094–1101.CrossRefGoogle Scholar
  9. Chorover, S. L., & Schiller, P. H. (1965). Short-term retrograde amnesia in rats. Journal of ­Comparative and Physiological Psychology, 59, 73–78.CrossRefPubMedGoogle Scholar
  10. Chuquet, J., Quilichini, P., Nimchinsky, E. A., & Buzsáki, G. (2010). Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. Journal of Neuroscience, 30, 15298–15303.PubMedCentralCrossRefPubMedGoogle Scholar
  11. Dornelles, A., de Lima, M. N. M., Grazziotin. M., Presti-Torres, J., Garcia, V. A., Scalco, F. S., Roesler, R., & Schröder, N. (2007). Adrenergic enhancement of consolidation of object recognition memory. Neurobiology of Learning and Memory, 88, 137–142.CrossRefPubMedGoogle Scholar
  12. Gaskin, S., & White, N. M. (2006). Cooperation and competition between the dorsal hippocampus and lateral amygdala in spatial discrimination learning. Hippocampus, 16, 577–585.CrossRefPubMedGoogle Scholar
  13. Ghanbarian, E., & Motamedi, F. (2013). Ventral tegmental area inactivation suppresses the ­expression of CA1 long term potentiation in anesthetized rat. PloS One, 8, e58844.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Gold, P. E. (1992). Modulation of memory processing: Enhancement of memory in rodents and humans. In L. R. Squire & N. Butters (Eds.), Neuropsychology of memory, (2nd Ed., pp. ­402–414). New York: Guilford.Google Scholar
  15. Gold, P. E. (1995). Modulation of emotional and non-emotional memories: Same pharmacological systems, different neuroanatomical systems. In J. L. McGaugh, N. M. Weinberger, & G. S. Lynch (Eds.), Brain and memory: Modulation and mediation of neural plasticity, (pp. 41–74). New York: Oxford University Press.CrossRefGoogle Scholar
  16. Gold, P. E. (2001). Drug enhancement of memory in aged rodents and humans. In: Carroll, M. E. & Overmier, J. B. (Eds.), Animal research and human health: Advancing human welfare through behavioral science, (pp. 293–304). Washington DC: American Psychological Association.CrossRefGoogle Scholar
  17. Gold, P. E. (2008). Protein synthesis inhibition: Memory formation vs. amnesia. Neurobiology of Learning and Memory, 89, 201–211.PubMedCentralCrossRefPubMedGoogle Scholar
  18. Gold, P. E., & Korol, D.L. (2010). Hormones and memory. In G. Koob, M. Le Moal, & R. F. Thompson (Eds.), Encyclopedia of behavioral neuroscience (Vol. 2, pp. 57–64). Oxford: ­Academic Press.CrossRefGoogle Scholar
  19. Gold, P. E., & Korol, D. L. (2012). Making memories matter. Special issue: The impact of emotion on cognition—dissociating between enhancing and impairing effects. F. Dolcos, L. Wang, and M. Mather, hosts. Frontiers in Integrative Neuroscience, 6, 116. doi:10.3389/fnint.2012.00116.PubMedCentralCrossRefPubMedGoogle Scholar
  20. Gold, P. E., & McGaugh, J. L. (1975). A single trace, two process view of memory storage ­processes. In: D. Deutsch & J. A. Deutsch (Eds.), Short term memory (pp. 355–390). New York: Academic Press.Google Scholar
  21. Gold, P. E., & Zornetzer, S. F. (1983). The mnemon and its juices: Neuromodulation of memory processes. Behavioral and Neural Biology, 38, 151–189,CrossRefPubMedGoogle Scholar
  22. Gold, P. E., Macri, J., & McGaugh, J. L. (1973). Retrograde amnesia gradients: Effects of direct cortical stimulation. Science, 197, 1343–1345.CrossRefGoogle Scholar
  23. Gold, P. E., Hankins, L., Edwards, R. M., Chester, J., & McGaugh, J. L. (1975). Memory interference and facilitation with posttrial amygdala stimulation: Effect on memory varies with ­footshock level. Brain Research, 86, 509–513.CrossRefPubMedGoogle Scholar
  24. Gold, P. E., Newman, L. A., Scavuzzo, C. J., & Korol, D. L. (2013). Modulation of multiple ­memory systems: From neurotransmitters to metabolic substrates. Hippocampus, 23, 1053–1065.CrossRefPubMedGoogle Scholar
  25. Gold, P. E., & van Buskirk, R. B. (1975). Facilitation of time dependent memory processes with posttrial epinephrine injections. Behavioral Biology, 13, 145–153.Google Scholar
  26. Gold, P. E., & van Buskirk, R. B. (1976). Effects of posttrial hormone injections on memory processes. Hormones and Behavior, 7, 509–517.Google Scholar
  27. Gold, P. E., van Buskirk, R. B., & Haycock, J. W. (1977). Effects of post training epinephrine injections on retention of avoidance training in mice. Behavioral Biology, 20, 197–204.Google Scholar
  28. Hall, J. L., Gonder-Frederick, L. A., Chewning, W. W., Silveira, J., & Gold, P. E. (1989). Glucose enhancement of performance on memory tests in young and aged humans. Neuropsychologia, 27, 1129–1138.CrossRefPubMedGoogle Scholar
  29. Huff, N. C., Wright-Hardesty, K. J., Higgins, E. A., Matus-Amat, P., & Rudy, J. W. (2005). Context pre-exposure obscures amygdala modulation of contextual-fear conditioning. Learning and Memory, 12, 456–460.CrossRefPubMedGoogle Scholar
  30. Jarrard, L. E., Isaacson, R. L., & Wickelgren, W. O. (1964). Effects of hippocampal ablation and intertrial interval on runway acquisition and extinction. Journal of Comparative and Physiological Psychology, 57, 442–444.CrossRefPubMedGoogle Scholar
  31. Kesner, R. P. (1985). Correspondence between humans and animals in coding of temporal ­attributes: Role of hippocampus and prefrontal cortex. Annals of the New York Academy of Science, 44, 122–136.CrossRefGoogle Scholar
  32. Kesner, R. P. (2009). Tapestry of memory. Behavioral Neuroscience, 123, 1–13.CrossRefPubMedGoogle Scholar
  33. Kesner, R. P., Bolland, B. L., & Dakis, M. (1993). Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate ­visual cortex. Experimental Brain Research, 93, 462–470.CrossRefPubMedGoogle Scholar
  34. Kleim, J. A., Bruneau, R., Calder, K., Pocock, D., VandenBerg, P. M., MacDonald, E., Monfils, M. H., Sutherland, R. J., & Nader, K. (2003). Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron, 40, 167–176.Google Scholar
  35. Korol, D. L. (2002). Enhancing cognitive function across the life span. Annals of the New York Academy of Science, 959, 167–179.CrossRefGoogle Scholar
  36. Korol, D. L., & Gold, P. E. (2007). Modulation of learning and memory by adrenal and ovarian hormones. In R. P. Kesner & J. L. Martinez (Eds.), Neurobiology of learning and memory (pp. 243–268). New York: Elsevier Science.CrossRefGoogle Scholar
  37. Korol, D. L., Gold, P. E., & Scavuzzo, C. J. (2013). Use it and boost it with physical and mental activity. Hippocampus, 23, 1125–1135.CrossRefPubMedGoogle Scholar
  38. Krebs, D. L., & Parent, M. B. (2005). The enhancing effects of hippocampal infusions of ­glucose are not restricted to spatial working memory. Neurobiology of Learning and Memory, 83, 168–172.CrossRefPubMedGoogle Scholar
  39. Mabry, T. R., Gold, P. E., & McCarty, R. (1995). Age-related changes in plasma catecholamine and glucose responses of F-344 rats to footshock as in inhibitory avoidance training. Neurobiology of Learning and Memory, 64, 146–155.CrossRefPubMedGoogle Scholar
  40. Manning, C. A., Hall, J. L., & Gold, P. E. (1990). Glucose effects on memory and other neuropsychological tests in elderly humans. Psychological Sciences, 1, 307–311.CrossRefGoogle Scholar
  41. Manning, C. A., Parsons, M. W., & Gold, P. E. (1992). Anterograde and retrograde enhancement of 24-hour memory by glucose in elderly humans. Behavioral and Neural Biology, 58, 125–130.CrossRefPubMedGoogle Scholar
  42. Manning, C. A., Ragozzino, M., & Gold, P. E. (1993). Glucose enhancement of memory in patients with Alzheimer’s disease. Neurobiology of Aging, 14, 523–528.CrossRefPubMedGoogle Scholar
  43. Manning, C. A., Parsons, M. W., Cotter, E. M., & Gold, P. E. (1997). Glucose effects on declarative and nondeclarative memory in healthy elderly and young adults. Psychobiology, 25, 103–108.Google Scholar
  44. Manning, C. A., Honn, V. S., Stone, W. S., Jane, J. S., & Gold, P. E. (1998). Glucose effects on cognition in adults with Down’s Syndrome. Neuropsychology, 12, 479–484.CrossRefPubMedGoogle Scholar
  45. Marriott, L. K., & Korol, D. L. (2003). Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning. Neurobiology of Learning and Memory, 80, 315–322.Google Scholar
  46. McDonald, R. J., & White, N. M. (1993). A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience, 107, 3–22.CrossRefPubMedGoogle Scholar
  47. McDonald, R. J., & White, N. M. (1995). Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat. Hippocampus, 5, 189–197.CrossRefPubMedGoogle Scholar
  48. McGaugh, J. L. (1966). Time-dependent processes in memory storage. Science, 153, 1351–1358.CrossRefPubMedGoogle Scholar
  49. McGaugh, J. L. (1983). Hormonal influences on memory. Annual Review Psychology, 34, 297–323.CrossRefGoogle Scholar
  50. McGaugh, J. L., & Roozendaal, B. (2002). Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion Neurobiology, 12, 205–210.CrossRefGoogle Scholar
  51. McHugh, T. J., & Tonegawa, S. (2007). Spatial exploration is required for the formation of contextual fear memory. Behavioral Neuroscience, 121, 335–339.CrossRefPubMedGoogle Scholar
  52. McIntyre, C. K., Marriott, L. K., & Gold, P. E. (2003a). Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiology of Learning and Memory, 79, 177–183CrossRefPubMedGoogle Scholar
  53. McIntyre, C. K., Marriott, L. K., & Gold, P. E. (2003b). Cooperation between memory systems: Acetylcholine release in the amygdala correlates positively with good performance on a hippocampus-dependent task. Behavioral Neuroscience, 117, 320–326.CrossRefPubMedGoogle Scholar
  54. McIntyre, C. K., Pal, S. N., Marriott, L. K., & Gold, P. E. (2002). Competition between memory systems: Acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. Journal of Neuroscience, 22, 1171–1176.PubMedGoogle Scholar
  55. McNay, E. C., & Gold, P. E. (2001). Age-related differences in hippocampal extracellular fluid glucose concentration during behavioral testing and following systemic glucose administration. Journal of Gerontology: Biological Sciences, 56A, B66–B71.Google Scholar
  56. McNay, E. C., & Sherwin, R. S. (2004). Effect of recurrent hypoglycemia on spatial cognition and cognitive metabolism in normal and diabetic rats. Diabetes, 53, 418–425.CrossRefPubMedGoogle Scholar
  57. McNay, E. C., Fries, T. M., & Gold, P. E. (2000). Decreases in rat extracellular hippocampal ­glucose concentration associated with cognitive demand during a spatial task. Proceedings of the National Academy of Science USA, 97, 2881–2885.CrossRefGoogle Scholar
  58. McNay, E. C., McCarty, R. M., & Gold, P. E. (2001). Fluctuations in glucose concentration during behavioral testing: Dissociations both between brain areas and between brain and blood. Neurobiology of Learning and Memory, 75, 325–337.CrossRefPubMedGoogle Scholar
  59. Means, L. W., Walker, D. W., & Isaacson, R. L. (1970). Facilitated single alternation go, no- go performance following hippocampectomy in the rat. Journal of Comparative and Physiological Psychology, 72, 278–285CrossRefPubMedGoogle Scholar
  60. Milner, B., Corkin, S., & Teuber, H. L. (1968). Further analysis of the hippocampal amnesic ­syndrome: 14-year follow-up study of HM. Neuropsychologia, 6, 215–234.CrossRefGoogle Scholar
  61. Morris, K. A., & Gold, P. E. (2013). Epinephrine and glucose modulate training-related CREB phosphorylation in old rats: Relationships to age-related memory impairments. Experimental Gerontology, 48, 115–127.PubMedCentralCrossRefPubMedGoogle Scholar
  62. Morris, K. A., Chang, Q., Mohler, E. G., & Gold, P. E. (2010). Age-related memory impairments due to reduced blood glucose responses to epinephrine. Neurobiology of Aging, 31, 2136–2145.PubMedCentralCrossRefPubMedGoogle Scholar
  63. Naeem, M., & White, N. M. (2011). Lesions of basolateral and central amygdala differentiate conditioned cue preference learning with and without unreinforced preexposure. Behavioral Neuroscience, 125, 84–92.CrossRefPubMedGoogle Scholar
  64. Newcomer, J. W., Craft, S., Fucetola, R., Moldin, S. O., Selke, G., Paras, L., & Miller, R. (1999). Glucose-induced increase in memory performance in patients with schizophrenia. Schizophrenia Bulletin, 25, 321–335.CrossRefPubMedGoogle Scholar
  65. Newman, L. A., Korol, D. L., & Gold, P. E. (2011). Lactate produced by glycogenolysis in ­astrocytes regulates memory. PLoS One, 6, e28427.PubMedCentralCrossRefPubMedGoogle Scholar
  66. Nicoll, R. A., & Roche, K. W. (2013). Long-term potentiation: Peeling the onion. Neuropharmacology, 74, 18–22.PubMedCentralCrossRefPubMedGoogle Scholar
  67. Packard, M. G. (1999). Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proceedings of the National Academy of Science USA, 96, 12881–12886.CrossRefGoogle Scholar
  68. Packard, M. G., & Cahill, L. (2001). Affective modulation of multiple memory systems. Current Opinion in Neurobiology, 11, 752–756.CrossRefPubMedGoogle Scholar
  69. Packard, M. G., & McGaugh, J. L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory, 65, 65–72.CrossRefPubMedGoogle Scholar
  70. Paolino, R. M., Quartermain, D., & Miller, N. E. (1966). Different temporal gradients of retrograde amnesia produced by carbon dioxide anesthesia and electroconvulsive shock. Journal of ­Comparative and Physiological Psychology, 62, 270–274.CrossRefPubMedGoogle Scholar
  71. Parsons, M., & Gold, P. E. (1992). Glucose enhancement of memory in elderly humans: An inverted-U dose-response curve. Neurobiology of Aging, 13, 401–404.CrossRefPubMedGoogle Scholar
  72. Poldrack, R. A., & Packard, M. G. (2003). Competition among multiple memory systems: ­Converging evidence from animal and human brain studies. Neuropsychologia, 41, 245–251.CrossRefPubMedGoogle Scholar
  73. Pych, J. C., Chang, Q., Colon-Rivera, C., & Gold, P. E. (2005a). Acetylcholine release in hippocampus and striatum during training on a rewarded spontaneous alternation task. Neurobiology of Learning and Memory, 84, 93–101.CrossRefPubMedGoogle Scholar
  74. Pych, J. C., Chang, Q., Colon-Rivera, C., Haag, R., & Gold, P. E. (2005b). Acetylcholine release in the hippocampus and striatum during place and response training. Learning and Memory, 12, 564–572.PubMedCentralCrossRefPubMedGoogle Scholar
  75. Pych, J. C., Kim, M., & Gold, P. E. (2006). Effects of injections of glucose into the dorsal striatum on learning of place and response mazes. Behavioural Brain Research, 167, 373–378.CrossRefPubMedGoogle Scholar
  76. Qi, Z., & Gold, P. E. (2009). Intrahippocampal infusions of anisomycin produce amnesia: ­Contributions of increased release of norepinephrine, dopamine and acetylcholine. Learning and Memory, 16, 308–314.PubMedCentralCrossRefPubMedGoogle Scholar
  77. Quartermain, D., Paolino, R. M., & Miller, N. E. (1965). A brief temporal gradient of retrograde amnesia independent of situational change. Science, 149, 1116–1118.CrossRefPubMedGoogle Scholar
  78. Ragozzino, M. E., Unick, K. E., & Gold, P. E. (1996). Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proceedings of the National Academy of Science USA, 93, 4693–4698.CrossRefGoogle Scholar
  79. Ragozzino, M. E., Pal, S. N., Unick, K., Stefani, M. R., & Gold, P. E. (1998). Modulation of ­hippocampal acetylcholine release and of memory by intrahippocampal glucose injections. Journal of Neuroscience, 18, 1595–1601.PubMedGoogle Scholar
  80. Restle, F. (1957). Discrimination of cues in mazes: A resolution of the place-vs.- response ­question. Psychological Review, 64, 217–228.CrossRefPubMedGoogle Scholar
  81. Routtenberg, A. (2013). Lifetime memories from persistently supple synapses. Hippocampus, 2, 202–206.CrossRefGoogle Scholar
  82. Routtenberg, A., & Rekart, J. L. (2005). Post-translational protein modification as the substrate for long-lasting memory. Trends in Neuroscience, 28, 12–19.CrossRefGoogle Scholar
  83. Rudy, J. W., & Matus-Amat, P. (2005). The ventral hippocampus supports a memory representation of context and contextual fear conditioning: Implications for a unitary function of the hippocampus. Behavioral Neuroscience, 119, 154–163CrossRefPubMedGoogle Scholar
  84. Rudy, J. W., Barrientos, R. M., & O’Reilly, R. C. (2002). Hippocampal formation supports ­conditioning to memory of a context. Behavioral Neuroscience, 116, 530–538.CrossRefPubMedGoogle Scholar
  85. Salado-Castillo, R., Guante, M. A., Alvarado, R., Quirarte, G. L., & Prado-Alcalá, R. A. (1996). Effects of regional GABAergic blockade of the striatum on memory consolidation. Neurobiology of Learning and Memory, 66, 102–108.CrossRefPubMedGoogle Scholar
  86. Schroeder, J. P., & Packard, M. G. (2003). Systemic or intra-amygdala injections of glucose ­facilitate memory consolidation for extinction of drug-induced conditioned reward. European Journal of Neuroscience, 17, 1482–1488.CrossRefPubMedGoogle Scholar
  87. Sharma, A. V., Nargang, F. E., & Dickson, C. T. (2012). Neurosilence: Profound suppression of neural activity following intracerebral administration of the protein synthesis inhibitor ­anisomycin. Journal of Neuroscience, 32, 2377–2387.CrossRefPubMedGoogle Scholar
  88. Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195–231.CrossRefPubMedGoogle Scholar
  89. Squire, L. R., & Spanis, C. W. (1984). Long gradient of retrograde amnesia in mice: Continuity with the findings in humans. Behavioral Neuroscience, 98, 345–348.CrossRefPubMedGoogle Scholar
  90. Squire, L. R., Slater, P. C., & Chace, P. M. (1975). Retrograde amnesia: Temporal gradient in very long term memory following electroconvulsive therapy. Science, 187, 77–79.CrossRefPubMedGoogle Scholar
  91. Stefani, M. R., & Gold, P. E. (1998). Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Research, 813, 50–56.CrossRefPubMedGoogle Scholar
  92. Sternberg, D. B., Isaacs, K., Gold, P. E., & McGaugh, J. L. (1985). Epinephrine facilitation of appetitive learning: Attenuation with adrenergic receptor antagonists. Behavioral and Neural Biology, 44, 447–453.CrossRefPubMedGoogle Scholar
  93. Stone, W. S., & Seidma, L. J. (2008). Toward a model of memory enhancement in schizophrenia: Glucose administration and hippocampal function. Schizophrenia Bulletin, 34, 93–108.PubMedCentralCrossRefPubMedGoogle Scholar
  94. Stone, W. S., Seidman, L. J., Wojcik, J. D., & Green, A. I. (2003). Glucose effects on cognition in schizophrenia. Schizophrenia Research, 62, 93–103.CrossRefPubMedGoogle Scholar
  95. Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., & Alberini, C. M. (2011). Astrocyte-neuron lactate transport is required for long-term memory formation. Cell, 144, 810–823.PubMedCentralCrossRefPubMedGoogle Scholar
  96. Talley, C. E. P., Kahn, S., Alexander, L., & Gold, P.E. (2000). Epinephrine fails to enhance performance of food-deprived rats on a delayed spontaneous alternation task. Neurobiology of Learning and Memory, 73, 79–86.Google Scholar
  97. Thomas, G. J. (1971). Maze retention by rats with hippocampal lesions and with fornicotomies. Journal of Comparative and Physiological Psychology, 75, 41–49.CrossRefPubMedGoogle Scholar
  98. Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55, 189–208.CrossRefPubMedGoogle Scholar
  99. Villers, A., Godaux, E., & Ris, L. (2012). Long-lasting LTP requires neither repeated trains for its induction nor protein synthesis for its development. PLoS One, 7, e40823.PubMedCentralCrossRefPubMedGoogle Scholar
  100. Walker, D. W., Messer, L. G., Freund, G., & Means, L. W. (1972). Effect of hippocampal lesions and intertrial interval on single-alternation performance in the rat. Journal of Comparative and Physiological Psychology, 80, 469–477.CrossRefPubMedGoogle Scholar
  101. White, N. M. (2008). Multiple memory systems in the brain: Cooperation and competition. In H. B. Eichenbaum (Ed.), Memory systems of Byrne, J., editor, Learning and memory: A comprehensive reference (Vol 3, pp. 9–46). Oxford: Elsevier.CrossRefGoogle Scholar
  102. White, N. M., & McDonald, R. J. (1993). Acquisition of a spatial conditioned place preference is impaired by amygdala lesions and improved by fornix lesions. Behavioural Brain Research, 55, 269–281.CrossRefPubMedGoogle Scholar
  103. White, N. M., & McDonald, R. J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory, 77, 125–184.CrossRefPubMedGoogle Scholar
  104. Zornetzer, S. F., & Gold, M. S. (1976). The locus coeruleus: Its possible role in memory consolidation. Physiology & Behavior, 16, 331–336.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of BiologySyracuse UniversitySyracuseUSA

Personalised recommendations