Characteristics of the functioning of the hippocampal formation in waking and paradoxical sleep

Neuroscience and Behavioral Physiology

Volumn 39, Issue 6, 2009, Pages 523-534

  Sil'kis, Isa G ^a  

^a INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

Author keywords

Hippocampal formation; Neuromodulation; Paradoxical sleep; Synaptic plasticity

Indexed keywords

ACETYLCHOLINE; DOPAMINE; HYDROCORTISONE; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN;

ARTICLE; BRAIN FUNCTION; DENTATE GYRUS; HIPPOCAMPUS; HUMAN; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; PERFORANT NERVE TRACT; POLYSYNAPTIC REFLEX; PYRAMIDAL NERVE CELL; REM SLEEP; SIGNAL TRANSDUCTION; SUBICULUM; SYNAPTIC TRANSMISSION; WAKEFULNESS;

CORTICOSTERONE; DOPAMINE; HIPPOCAMPUS; HUMANS; MUSCARINE; NEURAL PATHWAYS; NEURONS; NOREPINEPHRINE; SEROTONIN; SLEEP, REM; SYNAPSES; SYNAPTIC TRANSMISSION; WAKEFULNESS;

EID: 67649311411     PISSN: 00970549     EISSN: 1573899X     Source Type: Journal    
DOI: 10.1007/s11055-009-9163-1     Document Type: Article

References (100)

1. O. S. Vinogradova, "Neuroscience at the end of the second millennium: A paradigm shift," Zh. Vyssh. Nerv. Deyat., 50, No. 5, 743-774 (2000).
2. I. G. Sil'kis, "A unified postsynaptic mechanism for the effects of various neuromodulators in modifying excitatory and inhibitory inputs to hippocampal neurons (a hypothesis)," Usp. Fiziol. Nauk., 33, No. 1, 40-56 (2002).
3. I. G. Sil'kis, "A possible mechanism for the influences of neuromodulators and modifiable inhibition on long-term potentiation and depression of excitatory inputs to hippocampal main neurons," Zh. Vyssh. Nerv. Deyat., 52, No. 4, 392-405 (2002).
4. V. G. Skrebitskii and A. N. Chepkova, "synaptic plasticity in relation to learning and memory," Usp. Fiziol. Nauk., 30, No. 1, 3-13 (1999).
5. D. N. Alfarez, O. Wiegert, M. Joëls, and H. J. Krugers, "Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation," Neurosci., 115, No. 4, 1119-1126 (2002).
6. A. Alonso and C. Kohler, "A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain," J. Comp. Neurol., 225, No. 3, 327-343 (1984).
7. J. M. Auerbach and M. Segal, "Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus," J. Physiol. (England), 492, No. 2, 479-493 (1996).
8. J. Behr, T. Gloveli, and U. Heinemann, "The perforant path projection from the medial entorhinal cortex layer III to the subiculum in the rat combined hippocampal-entorhinal cortex slice," Eur. J. Neurosci., 10, No. 3, 1011-1018 (1998).
9. M. Bijak, A. Zahorodna, and K. Tokarski, "Opposite effects of antidepressants and corticosterone on the sensitivity of hippocampal CA1 neurons to 5-HT1A and 5-HT4 receptor activation," Neunyn Schmiedebergs Arch. Pharmacol., 363, No. 5, 491-498 (2001).
10. T. Blank, R. Zwart, I. Nijholt, and J. Spiess, "Serotonin 5-HT2 receptor activation potentiates N-methyl-D-aspartate receptor-mediated ion currents by a protein kinase C-dependent mechanism," J. Neurosci. Res., 45, No. 1, 153-160 (1996).
11. R. D. Blitzer, O. Gil, and E. M. Landau, "Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus," Neurosci. Lett., 119, No. 2, 207-210 (1990).
12. V. Booth and G. R. Poe, "Input source and strength influences overall firing phase of model hippocampal CA1 pyramidal cells during theta: Relevance to REM sleep reactivation and memory consolidation," Hippocampus, 16, No. 2, 161-173 (2006).
13. J. Born and U. Wagner, "Memory consolidation during sleep: Role of cortisol feedback," Ann. N.Y. Acad. Sci., 1032, 198-201 (2004).
14. C. R. Bramham, K. Bacher-Svendsen, and J. M. Sarvey, "LTP in the lateral perforant path is beta-adrenergic receptor-dependent," Neuroreport, 8, No. 3, 719-724 (1997).
15. P. S. Buckmaster and P. A. Schwartzkroin, "Interneurons and inhibition in the dentate gyrus of the rat in vivo," J. Neurosci., 15, No. 1, 774-789 (1995).
16. E. C. Burgard, T. E. Cote, and J. M. Sarvey, "Muscarinic depression of synaptic transmission and blockade of norepinephrine-induced long-lasting potentiation in the dentate gyrus," Neurosci., 54, No. 2, 377-389 (1993).
17. E. C. Burgard and J. M. Sarvey, "Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyms," Neurosci. Lett., 116, No. 1-2, 34-39 (1990).
18. K. J. Canning, K. Wu, P. Peloquin, F. Kloosterman, and L. S. Leung, "Physiology of the entorhinal and perirhinal projections to the hippocampus studied by current source density analysis," Ann. N.Y. Acad. Sci., 911, 55-72 (2000).
19. D. A. Caruana, R. E. Sorge, J. Stewart, and C. A. Chapman, "Dopamine has bidirectional effects on synaptic responses to cortical inputs in layer II of the lateral entorhinal cortex," J. Neurophysiol., 96, No. 6, 3006-3015 (2006).
20. Z. Chen, K. Ito, S. Fujii, M. Miura, H. Furuse, H. Sasaki, K. Kaneko, H. Kato, and H. Miyakawa, "Roles of dopamine receptors in longterm depression: Enhancement via Dl receptors and inhibition via D2 receptors," Receptors Channels, 4, No. 1, 1-8 (1996).
21. M. Christ, M. Wehling, E. Kirsch, S. Viengchareun, M. C. Zennaro, and M. Lombes, "Enhancement of beta-adrenergic cAMP-signaling by the mineralocorticoid receptor," Mol. Cell Endocrinol., 231, No. 1-2, 23-31 (2005).
22. C. M. Colbert and W. B. Levy, "Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors," J. Neurophysiol., 68, No. 1, 1-8 (1992).
23. C. M. Colbert and W. B. Levy, "Long-term potentiation of perforant path synapses in hippocampal CA1 in vitro," Brain Res., 606, No. 1, 87-91 (1993).
24. L. V. Colom, A. Garcia-Hernandez, M. T. Castaneda, M. G. Perez-Cordova, and E. R. Garrido-Sanabria, "Septohippocampal networks in chronically epileptic rats: Potential antiepileptic effects of theta rhythm generation," J. Neurophysiol., 95, No. 6, 3645-3653 (2006).
25. S. Communs, J. Gigg, M. Anderson, and S. M. O'Mara, "The projection from hippocampal area CA1 to the subiculum sustains longterm potentiation," Neuroreport, 9, No. 5, 847-850 (1998).
26. S. Craig and S. Commins, "Plastic and metaplastic changes in the CA1 and subicular projections to the entorhinal cortex," Brain Res., 1147, No. 1, 124-139 (2007).
27. D. Dahl and J. M. Sarvey, "Beta-adrenergic agonist-induced longlasting synaptic modifications in hippocampal dentate gyrus require activation of NMDA receptors, but not electrical activation of afferents," Brain Res., 526, No. 2, 347-350 (1990).
28. S. Datta, V. Mavanji, J. Ulloor, and E. H. Patterson, "Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: A mechanism for sleep-dependent plasticity," J. Neurosci., 24, No. 6, 1416-1427 (2004).
29. S. Datta, D. F. Siwek, E. H. Patterson, and P. B. Cipolloni, "Localization of pontine PGO wave generation sites and their anatomical projections in the rat," Synapse, 30, No. 4, 409-423 (1998).
30. V. H. Do, C. O. Martinez, Jr., and B. E. Derrick, "Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo," J. Neurophysiol., 87, No. 2, 669-678 (2002).
31. R. M. Empson and U. Heinemann, "The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice," J. Physiol. (England), 484, No. 3, 707-720 (1995).
32. C. Gottesman, "The neurochemistry of waking and sleeping mental activity: The disinhibition-dopamine hypothesis," Psychiatry Clin. Neurosci., 56, No. 4, 345-354 (2002).
33. N. Hajos, E. C. Papp, L. Acsady, A. I. Levey, and T. F. Freund, "Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus," Neurosci., 82, No. 2, 355-376 (1998).
34. B. N. Hamam, M. Sinai, G. Poirier, and C. A. Chapman, "Cholinergic suppression of excitatory synaptic responses in layer II of the medial entorhinal cortex," Hippocampus, 17, No. 2, 103-113 (2007).
35. M. E. Hasselmo, E. Schnell, and E. Barkai, "Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3," J. Neurosci., 15, No. 7, 5249-5262 (1995).
36. U. Heinemann, D. Schmitz, C. Eder, and T. Gloveli, "Properties of entorhinal cortex projection cells to the hippocampal formation," Ann. N.Y. Acad. Sci., 911, 112-126 (2000).
37. J. A. Hobson, R. Stickgold, and E. F. Pace-Schott, "The neuropsychology of REM sleep dreaming," Neuroreport, 9, No. 3, R1-R4 (1998).
38. K. S. Hsu, "Characterization of dopamine receptors mediating inhibition of excitatory synaptic transmission in the rat hippocampal slice," J. Neurophysiol., 76, No. 3, 1887-1895 (1996).
39. Y. Y. Huang and E. R. Kandel, "Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors," Neuron, 16, No. 3, 611-617 (1996).
40. C.-C. Huang, Y.-C. Liang, and K.-S. Hsu, "A role of extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses," J. Neurosci., 19, No. 22, 9728-9738 (1999).
41. Y. Izumi and C. F. Zorumski, "Norepinephrine promotes long-term potentiation in the adult rat hippocampus in vitro," Synapse, 31, No. 3, 196-202 (1999).
42. D. Jaffe and D. Johnston, "Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule," J. Neurophysiol., 64, No. 3, 948-960 (1990).
43. J. John, M. F. Wu, L. N. Boehmer, and J. M. Siegel, "Cataplexyactive neurons in the hypothalamus: Implications for the role of histamine in sleep and waking behavior," Neuron, 42, No. 4, 619-634 (2004).
44. K. Kawa, "Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: A patch-clamp study," J. Neurophysiol., 71, No. 5, 1935-1947 (1994).
45. Y. J. Karten, W. Hesen, and M. Joels, "Serotonin and carbachol induced suppression of synaptic responses in rat CA1 hippocampal area: effects of corticosteroid receptor activation in vivo," Stress, 2, No. 3, 183-200 (1998).
46. T. Kimura, K. Ishihara, K. Ozawa, and M. Sasa, "Augmentation of serotonin-induced inhibition of neuronal activity in the hippocampus following repeated treatment with methamphetamine," Ann. N.Y. Acad. Sci., 1025, 242-247 (2004).
47. G. Klukowski and C. W. Harley, "Locus coeruleus activation induces perforant path-evoked population spike potentiation in the dentate gyrus of awake rat," Exptl. Brain Res., 102, No. 1, 165-170 (1994).
48. K. Kobayashi and H. Suzuki, "Dopamine selectively potentiates hippocampal mossy fiber to CA3 synaptic transmission," Neuropharmacology, 52, No. 2, 552-561 (2007).
49. K. Korz and J. U. Frey, "Stress-related modulation of hippocampal long-term potentiation in rats: Involvement of adrenal steroid receptors," J. Neurosci., 23, No. 19, 7281-7287 (2003).
50. K. A. Kosub, V. H. Do, and B. E. Derrick, "NMDA receptor antagonists block heterosynaptic long-term depression (LTD) but not long-term potentiation (LTP) in the CA3 region following lateral perforant path stimulation," Neurosci. Lett., 374, No. 1, 29-34 (2005).
51. A. Kulla and D. Manahan-Vaughan, "Depotentiation in the dentate gyrus of freely moving rats is modulated by D1/D5 dopamine receptors," Cereb. Cortex, 10, No. 6, 614-620 (2000).
52. A. Kunitake, T. Kunitake, and M. Stewart, "Differential modulation by carbachol of four separate excitatory afferent systems to the rat subiculum in vitro," Hippocampus, 14, No. 8, 986-999 (2004).
53. I. Lena, S. Parrot, O. Deschaux, S. Moffat-Joly, V. Sauvinet, B. Renaud, M. F. Suaud-Chagny, and C. Gottesmann, "Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep-wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats," J. Neurosci. Res., 81, No. 6, 891-899 (2005).
54. C. Leranth, D. Carpi, G. Buzsaki, and J. Kiss, "The entorhino-septosupramammillary nucleus connection in the rat: morphological basisof a feedback mechanism regulating hippocampal theta rhythm," Neurosci., 88, No. 3, 701-708 (1999).
55. C. Leranth, T. Deller, and G. Buzsaki, "Intraseptal connections redefined: Lack of a lateral septum to medial septum path," Brain Res., 583, No. 1-2, 1-11 (1992).
56. Y. Levkovitz and M. Segal, "Serotonin 5-HT1A receptors modulate hippocampal reactivity to afferent stimulation," J. Neurosci., 17, No. 14, 5591-5598 (1997).
57. W. B. Levy, N. L. Desmond, and D. Z. Zhang, "Perforant path activation modulates the induction of long-term potentiation of the Schäffer collateral-hippocampal CA1 response: Theoretical and experimental analyses," Learn. Mem., 4, No. 6, 510-518 (1998).
58. A. Y. Kiu, U. Walter, and P. Greengard, "Steroid hormones may regulate autophosphorylation of adenosine-3′, 5′-monophosphatedependent protein kinase in target tissues," Eur. J. Biochem., 114, No. 3, 539-548 (1981).
59. T. Maeda, S. Kaneko, and M. Satoh, "Bidirectional modulation of long-term potentiation by carbachol via M1 and M2 muscarinic receptors in guinea pig hippocampal mossy fiber-CA3 synapses," Brain Res., 619, No. 1-2, 324-330 (1993).
60. F. Marrosu, C. Portas, M. S. Mascia, M. A. Casu, M. Fa, M. Giagheddu, A. Imperato, and G. L. Gessa, "Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats," Brain Res., 671, No. 2, 329-332 (1995).
61. C. O. Martinez, V. H. Do, J. L. Martinez, Jr., and B. E. Derrick, "Associative long-term potentiation (LTP) among extrinsic afferents of the hippocampal CA3 region in vivo," Brain Res., 940, No. 1-2, 86-94 (2002).
62. D. B. McMahon and G. Barrionuevo, "Short- and long-term plasticity of the perforant path synapse in hippocampal area CA3," J. Neurophysiol., 88, No. 1, 528-533 (2002).
63. B. Mlinar, A. M. Pugliese, and R. Corradetti, "Selective inhibition of local excitatory synaptic transmission by serotonin through an unconventional receptor in the CA1 region of rat hippocampus," J. Physiol., 534, No. 1, 141-158 (2001).
64. K. Mori, H. Togashi, T. Kojima, M. Matsumoto, S. Ohashi, K. Ueno, and M. Yoshioka, "Different effects of anxiolytic agents, diazepam and 5-HT(1A) agonist tandospirone, on hippocampal long-term potentiation in vivo," Pharmacol. Biochem. Behav., 69, No. 3-4, 367-372 (2001).
65. Z. Muzur, "Toward an integrative theory of sleep and dreaming," J. Theor. Biol., 233, No. 1, 103-118 (2005).
66. K. Nakashima, H. Hayashi, O. Shimizu, and S. Ishizuka, "Longterm change in synaptic transmission in CA3 circuits followed by spontaneous rhythmic activity in rat hippocampal slices," Neurosci. Res., 40, No. 4, 325-336 (2001).
67. N. A. Otmakhova, J. Lewey, B. Asrican, and J. E. Lisman, "Inhibition of perforant path input to the CA1 region by serotonin and noradrenaline," J. Neurophysiol., 94, No. 2, 1413-1422 (2005).
68. N. A. Otmakhova and J. E. Lisman, "D1/D5 dopamine receptors inhibit depotentiation at CA1 synapses via cAMP-dependent mechanism," J. Neurosci., 18, No. 4, 1270-1279 (1998).
69. N. A. Otmakhova and J. E. Lisman, "Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region," J. Neurosci., 19, No. 4, 1437-1445 (1999).
70. N. A. Otmakhova and J. E. Lisman, "D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses," J. Neurosci., 16, No. 23, 7478-7486 (1996).
71. S. V. Ovsepian, R. Anwyl, and M. J. Rowan, "Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: In vivo study," Eur. J. Neurosci., 20, No. 5, 1267-1275 (2004).
72. P. D. Patel, J. F. Lopez, D. M. Lyons, S. Burke, M. Wallace, and A. F. Schatzberg, "Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain," J. Psychiat. Res., 34, No. 6, 383-392 (2000).
73. C. Pavlides and B. S. McEwen, "Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field," Brain Res., 851, No. 1-2, 204-214 (1999).
74. C. Pavlides, S. Ogawa, A. Kimura, and B. S. McEwen, "Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices," Brain Res., 738, No. 2, 229-235 (1996).
75. C. Pavlides, Y. Watanabe, A. M. Magarinos, and B. S. McEwen, "Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation," Neurosci., 68, No. 2, 387-394 (1995).
76. C. Pavlides, Y. Watanabe, and B. S. McEwen, "Effects of glucocorticoids on hippocampal long-term potentiation," Hippocampus, 3, No. 2, 183-192 (1993).
77. J. D. Payne and L. Nadel, "Sleep, dreams, and memory consolidation: the role of the stress hormone cortisol," Learn. Mem., 11, No. 6, 671-678 (2004).
78. M. Remondes and E. M. Schuman, "Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons," Nature, 416, No. 6882, 736-740 (2002).
79. S. T. Rouse, M. J. Marino, and L. T. Potter, "Muscarinic receptor subtypes involved in hippocampal circuits," Life Sci., 64, No. 6-7, 501-509 (1999).
80. A. M. Rush, M. J. Rowan, and R. Anwyl, "Application of N-methyl-D-aspartate induces long-term potentiation in the medial perforant path and long-term depression in the lateral perforant path of the rat dentate gyrus in vitro," Neurosci. Lett., 298, No. 3, 175-178 (2001).
81. 2+ entry," Brain Res., 701, No. 1-2, 249-254 (1995).
82. P. Seeman and H. H. Van Tol, "Dopamine receptor pharmacology," Trends Pharmacol. Sci., 15, No. 7, 264-270 (1994).
83. M. Segal and J. M. Auerbach, "Muscarinic receptors involved in hippocampal plasticity," Life Sci., 60, No. 13-14, 1085-1091 (1997).
84. Y. Shimoshige, T. Maeda, S. Kaneko, A. Akaike, and M. Satoh, "Involvement of M2 receptor in an enhancement of long-term potentiation by carbachol in Schaffer collateral-CA1 synapses of hippocampal slices," Neurosci. Res., 27, No. 2, 175-180 (1997).
85. J. W. Smythe, L. V. Colom, and B. H. Bland, "The extrinsic modulation of hippocampal theta depends on the co-activation of cholinergic and GABA-ergic medial septal inputs," Neurosci. Biobehav. Rev., 16, No. 3, 289-308 (1992).
86. L. W. Swanson, "The anatomical organization of septohippocampal projections," Ciba Found. Symp., 58, 25-48 (1977).
87. K. Toth, Z. Borhegyi, and T. F. Freund, "Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex," J. Neurosci., 13, No. 9, 3712-3724 (1993).
88. K. Toth, T. F. Freund, and R. Miles, "Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum," J. Physiol. (England), 500, No. 2, 463-474 (1997).
89. R. P. Vertes and B. Kocsis, "Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus," Neurosci., 81, No. 4, 893-926 (1997).
90. S. G. Walling, D. J. Nutt, M. D. Lalies, and C. W. Harley, "Orexin-A infusion in the locus ceruleus triggers norepinephrine (ME) release and NE-induced long-term potentiation in the dentate gyrus," J. Neurosci., 24, No. 34, 7421-7426 (2004).
91. R. Y. Wang and V. L. Arvanov, "M100907, a highly selective 5-HT2A receptor antagonist and a potential atypical antipsychotic drug, facilitates induction of long-term potentiation in area CA1 of the rat hippocampal slice," Brain Res., 779, No. 1-2, 309-313 (1998).
92. H. Widmer, L. Ferrigan, C. H. Favies, and S. R. Cobb, "Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons," Hippocampus, 16, No. 7, 617-628 (2006).
93. J. Winson and C. Abzug, "Neuronal transmission through hippocampal pathways dependent on behavior," J. Neurophysiol., 41, No. 3, 716-732 (1978).
94. M. P. Witter and D. G. Amaral, "Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex," J. Comp. Neurol., 307, No. 3, 437-459 (1991).
95. R. Wohrl, D. von Haebler, and U. Heinemann, "Low-frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal-entorhinal cortex slice preparation," Eur. J. Neurosci., 25, No. 1, 251-258 (2007).
96. C. H. Yang, C. C. Huang, and K. S. Hsu, "Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake," J. Neurosci., 25, No. 17, 4288-4293 (2005).
97. M. F. Yeckel and T. W. Berger, "Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: Redefinition of the role of the trisynaptic pathway," Proc. Natl. Acad. Sci. USA, 87, No. 15, 5832-5836 (1990).
98. M. F. Yeckel, A. Kapur, and D. Johnston, "Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism," Nat. Neurosci., 2, No. 7, 625-633 (1999).
99. W. P. Zhang, J. F. Guzowski, and S. A. Thomas, "Mapping neuronal activation and the influence, of adrenergic signaling during contextual memory retrieval," Learn. Mem., 12, No. 3, 239-247 (2005).
100. P. Zheng, X. X. Zhang, B. S. Bunney, and W. X. Shi, "Opposite modulation of cortical N-methyl-D-aspartate receptor-mediated responses by low and high concentrations of dopamine," Neurosci., 91, No. 2, 527-535 (1999).