慢性吗啡处理过程中小鼠海马CA1神经信息编码的改变
|
摘要
海马在空间记忆以及新记忆形成中起到重要的作用。最近,越来越多的证据表明海马也可能参与了药物成瘾的过程。因此,海马似乎是联系药物成瘾与学习记忆的重要的关联脑区。理论以及实验研究发现海马神经网络中不同频率的振荡运动,及其独特的发放模式在神经信息编码中扮演着重要的角色。这里,我们使用在体多通道神经信号记录系统,可以在动物清醒活动状态下记录海马CA1神经信息的编码,包括theta波(4-10Hz)和gamma波(40-100Hz)的相位关系,以及theta波和gamma波对CA1区不同神经元的调制。我们发现小鼠海马CA1局部场电位,以及单位放电模式在慢性吗啡处理后发生明显改变。吗啡处理后theta波的能量明显升高,同时在小鼠不同活动状态下theta波的锋频率也发生明显的移动。而且通过研究theta波和gamma波的相位关系发现,theta波和gamma波的相位也发生了移动,并且gamma波的锋频率也明显升高。但是有趣的是,gamma波的能量却没有明显改变。此外,我们也发现在吗啡处理后,锥体神经元与theta波的相位关系发生了移动,而在gamma波中的相位并未改变。而中间神经元与gamma波的相位关系有明显改变,在theta波中的相位却没有改变。为了进一步研究在慢性吗啡处理后影响海马CA1神经信息编码的可能因素,我们通过海马CA1内微注射技术,发现上面的神经信息编码的改变可以被多巴胺受体1的拮抗剂SCH23390明显抑制,而注射多巴胺受体2的拮抗剂以及吗啡受体拮抗剂纳洛酮并没有作用。我们的实验表明海马CA1神经信息编码模式在慢性吗啡处理中的改变参与了药物成瘾,并且这些神经发放模式的改变受海马内多巴胺调控。
The hippocampus plays an important role in the formation of new memories and spatial navigation. Recently, growing evidence supports the view that it is also involved in addiction to opiates and other drugs. Theoretical and experimental studies suggest that hippocampal neural-network oscillations at specific frequencies and unit firing patterns reflect information of learning and memory encoding. Here, using multichannel recordings from the hippocampal CAl area in behaving mice, we investigated the phase correlations between the theta (4-10 Hz) and gamma (40-100 Hz) oscillations, and the timing of spikes modulated by these oscillations. Local field potentials and single unit recordings in CAl area of mice receiving chronic morphine treatment revealed that the power of the theta rhythm was strongly increased, at the same time, the theta frequency during different behavioral states shifted markedly, and the characteristic coupling of theta and gamma oscillations was altered. Surprisingly, though the gamma oscillation frequency changed, its power did not. Moreover, the timing of pyramidal cell spikes relative to the theta rhythm and the timing of interneuron spikes relative to the gamma rhythm showed change during chronic morphine administration. Furthermore, both responses were dependent on local dopamine receptor activation, since they were impaired by a selective D1/D5 receptor antagonist. These results indicate that changes of ensemble activity in the CAl area caused by chronic morphine administration related to drug addiction.
The hippocampus plays an important role in the formation of new memories and spatial navigation. Recently, growing evidence supports the view that it is also involved in addiction to opiates and other drugs. Theoretical and experimental studies suggest that hippocampal neural-network oscillations at specific frequencies and unit firing patterns reflect information of learning and memory encoding. Here, using multichannel recordings from the hippocampal CAl area in behaving mice, we investigated the phase correlations between the theta (4-10 Hz) and gamma (40-100 Hz) oscillations, and the timing of spikes modulated by these oscillations. Local field potentials and single unit recordings in CAl area of mice receiving chronic morphine treatment revealed that the power of the theta rhythm was strongly increased, at the same time, the theta frequency during different behavioral states shifted markedly, and the characteristic coupling of theta and gamma oscillations was altered. Surprisingly, though the gamma oscillation frequency changed, its power did not. Moreover, the timing of pyramidal cell spikes relative to the theta rhythm and the timing of interneuron spikes relative to the gamma rhythm showed change during chronic morphine administration. Furthermore, both responses were dependent on local dopamine receptor activation, since they were impaired by a selective D1/D5 receptor antagonist. These results indicate that changes of ensemble activity in the CAl area caused by chronic morphine administration related to drug addiction.
引文
Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc NatlAcad SciU S A 107:3228-3233).
Bauer M, Oostenveld R, Peeters M, Fries P (Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490-501.2006).
Berke JD, Hyman SE (Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.2000).
Bliss TV, Collingridge GL (A synaptic model of memory:long-term potentiation in the hippocampus. Nature 361:31-39.1993).
Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.1995).
Bridger WH, Schiff SR, Cooper SS, Paredes W, Barr GA (Classical conditioning of cocaine's stimulatory effects. Psychopharmacol Bull 18:210-214.1982).
Buzsaki G (Theta oscillations in the hippocampus. Neuron 33:325-340.2002).
Buzsaki G, Eidelberg E (Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 266:334-339.1983).
Chrobak JJ, Buzsaki G (Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.1998).
Csicsvari J, Jamieson B, Wise KD, Buzsaki G (Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.2003).
del Olmo N, Miguens M, Higuera-Matas A, Torres I, Garcia-Lecumberri C, Solis JM, Ambrosio E (Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116:120-126.2006).
Dong Z, Han H, Wang M, Xu L, Hao W, Cao J (Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens. Hippocampus 16:809-813.2006a).
Dong Z, Zhong W, Tian M, Han H, Cao J, Xu T, Luo J, Xu L (Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo. Hippocampus 16:1017-1025.2006b).
Dragoi G, Buzsaki G (Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145-157.2006).
Eisch AJ, Harburg GC (Opiates, psychostimulants, and adult hippocampal neurogenesis: Insights for addiction and stem cell biology. Hippocampus 16:271-286.2006).
Everitt BJ, Robbins TW (Neural systems of reinforcement for drug addiction:from actions to habits to compulsion. Nat Neurosci 8:1481-1489.2005).
Fell J, Fernandez G, Elger CE (More than synchrony:EEG chaoticity may be necessary for conscious brain functioning. Med Hypotheses 61:158-160.2003).
Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.2001).
Fisher NI (Statistical Analysis of Circular Data. Cambridge University Press.1993).
Fries P, Neuenschwander S, Engel AK, Goebel R, Singer W (Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4:194-200.2001).
Gasbarri A, Packard MG, Campana E, Pacitti C (Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445-452.1994).
Gasbarri A, Sulli A, Packard MG (The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22.1997).
Hasselmo ME, Eichenbaum H (Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 18:1172-1190.2005).
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689-707.2002).
Holscher C (Long-term potentiation:a good model for learning and memory? Prog Neuropsychopharmacol Biol Psychiatry 21:47-68.1997).
Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, Schulze-Bonhage A, Kahana MJ (Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369-1374.2003).
Huang YY, Kandel ER (D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446-2450.1995).
Huerta PT, Lisman JE (Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.1993).
Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731.2003).
Hyman SE (Addiction:a disease of learning and memory. Am J Psychiatry 162:1414-1422.2005).
Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28:5959-5964.2008).
Jacobs J, Kahana MJ, Ekstrom AD, Fried I (Brain oscillations control timing of single-neuron activity in humans. J Neurosci 27:3839-3844.2007).
Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N (Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340-348.2008).
Jouvet M (Biogenic amines and the states of sleep. Science 163:32-41.1969).
Karami M, Zarrindast MR, Sepehri H, Sahraei H (Role of nitric oxide in the rat hippocampal CA1 area on morphine-induced conditioned place preference. Eur J Pharmacol 449:113-119.2002).
Kelley AE (Memory and addiction:shared neural circuitry and molecular mechanisms. Neuron 44:161-179.2004).
Lee H, Simpson GV, Logothetis NK, Rainer G (Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45:147-156.2005).
Leung LS (Fast (beta) rhythms in the hippocampus:a review. Hippocampus 2:93-98.1992).
Lisman JE, Idiart MA (Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267:1512-1515.1995).
Lu L, Zeng S, Liu D, Ceng X (Inhibition of the amygdala and hippocampal calcium/calmodulin-dependent protein kinase II attenuates the dependence and relapse to morphine differently in rats. Neurosci Lett 291:191-195.2000).
Malenka RC, Nicoll RA (Long-term potentiation—a decade of progress? Science 285:1870-1874.1999).
Martin PD, Shapiro ML (Disparate effects of long-term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats. Hippocampus 10:207-212.2000).
Masuoka T, Fujii Y, Kamei C (Participation of the hippocampal theta rhythm in memory formation for an eight-arm radial maze task in rats. Brain Res 1103:159-163.2006).
Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (Elements of a neurobiological theory of the hippocampus:the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.2003).
Nestler EJ (Neurobiology. Total recall-the memory of addiction. Science 292:2266-2267.2001).
O'Keefe J, Recce ML (Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.1993).
Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523-7531.2006).
Otmakhova NA, Lisman JE (D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.1996).
Panlilio LV, Schindler CW (Conditioned locomotor-activating and reinforcing effects of discrete stimuli paired with intraperitoneal cocaine. Behav Pharmacol 8:691-698.1997).
Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-1327.2008).
Penttonen M, Kamondi A, Acsady L, Buzsaki G (Gamma frequency oscillation in the hippocampus of the rat:intracellular analysis in vivo. Eur J Neurosci 10:718-728.1998).
Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811.2002).
Pu L, Bao GB, Xu NJ, Ma L, Pei G (Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914-1921.2002).
Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (Gating of human theta oscillations by a working memory task. J Neurosci 21:3175-3183.2001).
Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani A (Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 17:415-423.2003).
Robbins TW, Ersche KD, Everitt BJ (Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1-21.2008).
Robbins TW, Everitt BJ (Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:625-636.2002).
Salinas E, Sejnowski TJ (Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539-550.2001).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Dependence on morphine impairs the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Brain Res 965:108-113.2003a).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Long-term potentiation as an electrophysiological assay for morphine dependence and withdrawal in rats:an in vitro study. J Neurosci Methods 124:189-196.2003b).
Sato N, Yamaguchi Y (Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18:419-424.2007).
Siapas AG, Lubenov EV, Wilson MA (Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.2005).
Skaggs WE, McNaughton BL (Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.1996).
Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.1996).
Stevens KE, Shiotsu G, Stein L (Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region. Brain Res 545:8-16.1991).
Tallon-Baudry C, Bertrand O, Henaff MA, Isnard J, Fischer C (Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 15:654-662.2005).
Thompson AM, Gosnell BA, Wagner JJ (Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42:1039-1042.2002).
Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H (Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad SciU S A.2009).
Vanderwolf CH (Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.1969).
Vetulani J (Drug addiction. Part II. Neurobiology of addiction. Pol J Pharmacol 53:303-317.2001).
Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL (Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-1178.2001).
Way EL, Loh HH, Shen FH (Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 167:1-8.1969).
White NM (Addictive drugs as reinforcers:multiple partial actions on memory systems. Addiction 91:921-949; discussion 951-965.1996).
Woolverton WL, Johnson KM (Neurobiology of cocaine abuse. Trends Pharmacol Sci 13:193-200.1992).
Zhong WX, Dong ZF, Tian M, Cao J, Xu L, Luo JH (N-methyl-D-aspartate receptor-dependent long-term potentiation in CA1 region affects synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. Neuroscience 141:1399-1413.2006).
Amaral DL (ed.) (2006) The Hippocampus Book:Oxford University Press.
Axmacher N, Haupt S, Fernandez G, Elger CE, Fell J (The role of sleep in declarative memory consolidation-direct evidence by intracranial EEG Cereb Cortex 18:500-507.2008).
Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A 107:3228-3233).
Bauer M, Oostenveld R, Peeters M, Fries P (Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490-501.2006).
Bennett TL, Hebert PN, Moss DE (Hippocampal theta activity and the attention component of discrimination learning. Behav Biol 8:173-181.1973).
Bergson C, Levenson R, Goldman-Rakic PS, Lidow MS (Dopamine receptor-interacting proteins: the Ca(2+) connection in dopamine signaling. Trends Pharmacol Sci 24:486-492.2003).
Berke JD, Hyman SE (Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.2000).
Best PJ, White AM (Placing hippocampal single-unit studies in a historical context. Hippocampus 9:346-351.1999).
Biala G, Betancur C, Mansuy 1M, Giros B (The reinforcing effects of chronic D-amphetamine and morphine are impaired in a line of memory-deficient mice overexpressing calcineurin. Eur J Neurosci 21:3089-3096.2005).
Black YD, Green-Jordan K, Eichenbaum HB, Kantak KM (Hippocampal memory system function and the regulation of cocaine self-administration behavior in rats. Behav Brain Res 151:225-238.2004).
Bliss TV, Collingridge GL (A synaptic model of memory:long-term potentiation in the hippocampus. Nature 361:31-39.1993).
Boyer P, Phillips JL, Rousseau FL, Ilivitsky S (Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res Rev 54:92-112.2007).
Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.1995).
Brankack J, Stewart M, Fox SE (Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310-327.1993).
Brazell MP, Mitchell SN, Gray JA (Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats:a dose-response and antagonist study. Neuropharmacology 30:823-833.1991).
Breese CR, Hampson RE, Deadwyler SA (Hippocampal place cells:stereotypy and plasticity. J Neurosci 9:1097-1111.1989).
Bridger WH, Schiff SR, Cooper SS, Paredes W, Barr GA (Classical conditioning of cocaine's stimulatory effects. Psychopharmacol Bull 18:210-214.1982).
Burke SN, Barnes CA (Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30-40.2006).
Buzsaki G (Theta oscillations in the hippocampus. Neuron 33:325-340.2002).
Buzsaki G (2006) Rhythms of the Brain:Oxford University Press.
Buzsaki G, Eidelberg E (Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 266:334-339.1983).
Buzsaki G, Laszlovszky I, Lajtha A, Vadasz C (Spike-and-wave neocortical patterns in rats:genetic and aminergic control. Neuroscience 38:323-333.1990).
Castro NG, de Mello MC, de Mello FG, Aracava Y (Direct inhibition of the N-methyl-D-aspartate receptor channel by dopamine and (+)-SKF38393. Br J Pharmacol 126:1847-1855.1999).
Chao SZ, Ariano MA, Peterson DA, Wolf ME (Dl dopamine receptor stimulation increases GluRl surface expression in nucleus accumbens neurons. J Neurochem 83:704-712.2002a).
Chao SZ, Lu W, Lee HK, Huganir RL, Wolf ME (D(1) dopamine receptor stimulation increases GluRl phosphorylation in postnatal nucleus accumbens cultures. J Neurochem 81:984-992.2002b).
Chrobak JJ, Buzsaki G (Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.1998).
Csicsvari J, Jamieson B, Wise KD, Buzsaki G (Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.2003).
Davidson TL, Jarrard LE (A role for hippocampus in the utilization of hunger signals. Behav Neural Biol 59:167-171.1993).
Deadwyler SA, West M, Lynch G (Activity of dentate granule cells during learning:differentiation of perforant path input. Brain Res 169:29-43.1979).
del Olmo N, Miguens M, Higuera-Matas A, Torres I, Garcia-Lecumberri C, Solis JM, Ambrosio E (Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116:120-126.2006).
Diana RA, Yonelinas AP, Ranganath C (Imaging recollection and familiarity in the medial temporal lobe:a three-component model. Trends Cogn Sci 11:379-386.2007).
Dong Z, Han H, Wang M, Xu L, Hao W, Cao J (Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens. Hippocampus 16:809-813.2006a).
Dong Z, Zhong W, Tian M, Han H, Cao J, Xu T, Luo J, Xu L (Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo. Hippocampus 16:1017-1025.2006b).
Dragoi G, Buzsaki G (Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145-157.2006).
Eichenbaum H, Yonelinas AP, Ranganath C (The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123-152.2007).
Eisch AJ, Harburg GC (Opiates, psychostimulants, and adult hippocampal neurogenesis:Insights for addiction and stem cell biology. Hippocampus 16:271-286.2006).
Ekstrom A, Viskontas I, Kahana M, Jacobs J, Upchurch K, Bookheimer S, Fried I (Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus 17:606-617.2007).
Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (Cellular networks underlying human spatial navigation. Nature 425:184-188.2003).
Everitt BJ, Robbins TW (Neural systems of reinforcement for drug addiction:from actions to habits to compulsion. Nat Neurosci 8:1481-1489.2005).
Fell J, Fernandez G, Elger CE (More than synchrony:EEG chaoticity may be necessary for conscious brain functioning. Med Hypotheses 61:158-160.2003).
Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.2001).
Fenton AA, Muller RU (Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U S A 95:3182-3187.1998).
Fiorentini C, Rizzetti MC, Busi C, Bontempi S, Collo G, Spano P, Missale C (Loss of synaptic D1 dopamine/N-methyl-D-aspartate glutamate receptor complexes in L-DOPA-induced dyskinesia in the rat. Mol Pharmacol 69:805-812.2006).
Fisher NI (Statistical Analysis of Circular Data. Cambridge University Press.1993).
Floresco SB, Blaha CD, Yang CR, Phillips AG (Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine:cellular mechanisms of input selection. J Neurosci 21:2851-2860.2001).
Freund RK, Luntz-Leybman V, Collins AC (Nicotine interferes with GABA-mediated inhibitory processes in mouse hippocampus. Brain Res 527:286-291.1990).
Fries P, Neuenschwander S, Engel AK, Goebel R, Singer W (Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4:194-200.2001).
Fukuda M, Kobayashi T, Bures J, Ono T (Rat exploratory behavior controlled by intracranial self-stimulation improves the study of place cell activity. J Neurosci Methods 44:121-131.1992).
Gasbarri A, Packard MG, Campana E, Pacitti C (Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445-452.1994a).
Gasbarri A, Sulli A, Packard MG (The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22.1997).
Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat:a combined retrograde tracing and immunohistochemical study. Brain Res 668:71-79.1994b).
Grace AA, Moore H, O'Donnell P (The modulation of corticoaccumbens transmission by limbic afferents and dopamine:a model for the pathophysiology of schizophrenia. Adv Pharmacol 42:721-724.1998).
Hallett PJ, Spoelgen R, Hyman BT, Standaert DG, Dunah AW (Dopamine Dl activation potentiates striatal NMDA receptors by tyrosine phosphorylation-dependent subunit trafficking. J Neurosci 26:4690-4700.2006).
Hasselmo ME, Eichenbaum H (Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 18:1172-1190.2005).
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689-707.2002).
Hirsh R, Davis RE, Holt L (Fornix—thalamus fibers, motivational states, and contextual retrieval. Exp Neurol 65:373-390.1979).
Hirsh R, Holt L, Mosseri A (Hippocampal mossy fibers, motivational states, and contextual retrieval. Exp Neurol 62:68-79.1978a).
Hirsh R, Leber B, Gillman K (Fornix fibers and motivational states as controllers of behavior:a study stimulated by the contextual retrieval theory.Behav Biol 22:463-478.1978b).
Holscher C (Long-term potentiation:a good model for learning and memory? Prog Neuropsychopharmacol Biol Psychiatry 21:47-68.1997).
Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, Schulze-Bonhage A, Kahana MJ (Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369-1374.2003).
Huang YY, Kandel ER (D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446-2450.1995).
Huang YY, Kandel ER, Varshavsky L, Brandon EP, Qi M, Idzerda RL, McKnight GS, Bourtchouladze R (A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83:1211-1222.1995).
Huerta PT, Lisman JE (Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.1993).
Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731.2003).
Hyman SE (Addiction:a disease of learning and memory. Am J Psychiatry 162:1414-1422.2005).
Imperato A, Obinu MC, Gessa GL (Effects of cocaine and amphetamine on acetylcholine release in the hippocampus and caudate nucleus. Eur J Pharmacol 238:377-381.1993).
Ito K, Abekawa T, Koyama T (Valproate blocks high-dose methamphetamine-induced behavioral cross-sensitization to locomotion-inducing effect of dizocilpine (MK-801), but not methamphetamine. Psychopharmacology (Berl) 186:525-533.2006).
Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28:5959-5964.2008).
Izquierdo I, da Cunha C, Rosat R, Jerusalinsky D, Ferreira MB, Medina JH (Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav Neural Biol 58:16-26.1992).
Jacobs J, Hwang G, Curran T, Kahana MJ (EEG oscillations and recognition memory:theta correlates of memory retrieval and decision making. Neuroimage 32:978-987.2006).
Jacobs J, Kahana MJ, Ekstrom AD, Fried I (Brain oscillations control timing of single-neuron activity in humans. J Neurosci 27:3839-3844.2007).
Jacobs LF (The evolution of the cognitive map. Brain Behav Evol 62:128-139.2003).
Jay TM (Dopamine:a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69:375-390.2003).
Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N (Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340-348.2008).
Jouvet M (Biogenic amines and the states of sleep. Science 163:32-41.1969).
Kaphzan H, O'Riordan KJ, Mangan KP, Levenson JM, Rosenblum K (NMDA and dopamine converge on the NMDA-receptor to induce ERK activation and synaptic depression in mature hippocampus. PLoS One 1:el38.2006).
Karami M, Zarrindast MR, Sepehri H, Sahraei H (Role of nitric oxide in the rat hippocampal CA1 area on morphine-induced conditioned place preference. Eur J Pharmacol 449:113-119.2002).
Kelley AE (Memory and addiction:shared neural circuitry and molecular mechanisms. Neuron 44:161-179.2004).
Kelly C, McCreadie RG (Smoking habits, current symptoms, and premorbid characteristics of schizophrenic patients in Nithsdale, Scotland. Am J Psychiatry 156:1751-1757.1999).
Knierim JJ, McNaughton BL (Hippocampal place-cell firing during movement in three-dimensional space. J Neurophysiol 85:105-116.2001).
Lavenex P, Amaral DG (Hippocampal-neocortical interaction:a hierarchy of associativity. Hippocampus 10:420-430.2000).
Lee FJ, Xue S, Pei L, Vukusic B, Chery N, Wang Y, Wang YT, Niznik HB, Yu XM, Liu F (Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine Dl receptor. Cell 111:219-230.2002).
Lee H, Simpson GV, Logothetis NK, Rainer G (Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45:147-156.2005).
Leung LS (Fast (beta) rhythms in the hippocampus:a review. Hippocampus 2:93-98.1992).
Liang D, Shi X, Qiao Y, Angst MS, Yeomans DC, Clark JD (Chronic morphine administration enhances nociceptive sensitivity and local cytokine production after incision. Mol Pain 4:7.2008).
Linseman MA, Corrigall WA (Effects of morphine on CA1 versus dentate hippocampal field potentials following systemic administration in freely-moving rats. Neuropharmacology 21:361-366.1982).
Lisman JE, Grace AA (The hippocampal-VTA loop:controlling the entry of information into long-term memory. Neuron 46:703-713.2005).
Lisman JE, Idiart MA (Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267:1512-1515.1995).
Liu Y, Sun QA, Chen Q, Lee TH, Huang Y, Wetsel WC, Michelotti GA, Sullenger BA, Zhang X (Targeting inhibition of GluRl Ser845 phosphorylation with an RNA aptamer that blocks AMPA receptor trafficking. J Neurochem 108:147-157.2009).
Lu L, Zeng S, Liu D, Ceng X (Inhibition of the amygdala and hippocampal calcium/calmodulin-dependent protein kinase II attenuates the dependence and relapse to morphine differently in rats. Neurosci Lett 291:191-195.2000).
Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD (Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A97:4398-4403.2000).
Maldonado R, Blendy JA, Tzavara E, Gass P, Roques BP, Hanoune J, Schutz G (Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273:657-659.1996).
Malenka RC, Nicoll RA (Long-term potentiation-a decade of progress? Science 285:1870-1874.1999).
Martin PD, Shapiro ML (Disparate effects of long-term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats. Hippocampus 10:207-212.2000).
Masuoka T, Fujii Y, Kamei C (Participation of the hippocampal theta rhythm in memory formation for an eight-arm radial maze task in rats. Brain Res 1103:159-163.2006).
Meyers RA, Zavala AR, Neisewander JL (Dorsal, but not ventral, hippocampal lesions disrupt cocaine place conditioning. Neuroreport 14:2127-2131.2003).
Meyers RA, Zavala AR, Speer CM, Neisewander JL (Dorsal hippocampus inhibition disrupts acquisition and expression, but not consolidation, of cocaine conditioned place preference. Behav Neurosci 120:401-412.2006).
Mitchell SN, Brazell MP, Joseph MH, Alavijeh MS, Gray JA (Regionally specific effects of acute and chronic nicotine on rates of catecholamine and 5-hydroxytryptamine synthesis in rat brain. Eur J Pharmacol 167:311-322.1989).
Mizuki Y, Tanaka M, Isozaki H, Nishijima H, Inanaga K (Periodic appearance of theta rhythm in the frontal midline area during performance of a mental task. Electroencephalogr Clin Neurophysiol 49:345-351.1980).
Morris RG, Garrud P, Rawlins JN, O'Keefe J (Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.1982).
Morris RG, Moser El, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (Elements of a neurobiological theory of the hippocampus:the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.2003).
Moser MB, Moser El (Functional differentiation in the hippocampus. Hippocampus 8:608-619.1998).
Nestler EJ (Neurobiology. Total recall-the memory of addiction. Science 292:2266-2267.2001).
O'Carroll CM, Morris RG (Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47:324-332.2004).
O'Keefe J, Recce ML (Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.1993).
Ohno M, Shibata S, Yamamoto T, Watanabe S (Working memory deficits following muscarinic blockade combined with depletion of brain somatostatin in rats. Brain Res 610:348-353.1993).
Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523-7531.2006).
Otmakhova NA, Lisman JE (D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.1996).
Panlilio LV, Schindler CW (Conditioned locomotor-activating and reinforcing effects of discrete stimuli paired with intraperitoneal cocaine. Behav Pharmacol 8:691-698.1997).
Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-1327.2008).
Pennartz CM, Groenewegen HJ, Lopes da Silva FH (The nucleus accumbens as a complex of functionally distinct neuronal ensembles:an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719-761.1994).
Penttonen M, Kamondi A, Acsady L, Buzsaki G (Gamma frequency oscillation in the hippocampus of the rat:intracellular analysis in vivo. Eur J Neurosci 10:718-728.1998).
Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811.2002).
Pu L, Bao GB, Xu NJ, Ma L, Pei G (Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914-1921.2002).
Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (Gating of human theta oscillations by a working memory task. J Neurosci 21:3175-3183.2001).
Rector DM, Poe GR, Harper RM (Imaging of hippocampal and neocortical neural activity following intravenous cocaine administration in freely behaving cats. Neuroscience 54:633-641.1993).
Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani A (Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 17:415-423.2003).
Ridley RM, Aitken DM, Baker HF (Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus. Brain Res 502:306-318.1989).
Robbins TW, Ersche KD, Everitt BJ (Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1-21.2008).
Robbins TW, Everitt BJ (Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:625-636.2002).
Salinas E, Sejnowski TJ (Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539-550.2001).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Dependence on morphine impairs the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Brain Res 965:108-113.2003a).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Long-term potentiation as an electrophysiological assay for morphine dependence and withdrawal in rats:an in vitro study. J Neurosci Methods 124:189-196.2003b).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M, Kazemnejad A (Dependence on morphine leads to a prominent sharing among the different mechanisms of long-term potentiation in the CA1 region of rat hippocampus. Brain Res 963:93-100.2003c).
Sato N, Yamaguchi Y (Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18:419-424.2007).
Schridde U, van Luijtelaar G (The role of hippocampal theta activity in sensory gating in the rat. Physiol Behav 74:257-266.2001).
Scoville WB, Milner B (Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.1957).
Seamans JK, Yang CR (The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58.2004).
Sharp PE, McNaughton BL, Barnes CA (Enhancement of hippocampal field potentials in rats exposed to a novel, complex environment. Brain Res 339:361-365.1985).
Siapas AG, Lubenov EV, Wilson MA (Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.2005).
Silverstone PH, Done C, Sharp T (In vivo monoamine release during naloxone-precipitated morphine withdrawal. Neuroreport 4:1043-1045.1993).
Skaggs WE, McNaughton BL (Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.1996).
Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.1996).
Spielewoy C, Gonon F, Roubert C, Fauchey V, Jaber M, Caron MG, Roques BP, Hamon M, Betancur C, Maldonado R, Giros B (Increased rewarding properties of morphine in dopamine-transporter knockout mice. Eur J Neurosci 12:1827-1837.2000).
Stevens KE, Shiotsu G, Stein L (Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region. Brain Res 545:8-16.1991).
Sutherland GR, McNaughton B (Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180-186.2000).
Tallon-Baudry C, Bertrand O, Henaff MA, Isnard J, Fischer C (Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 15:654-662.2005).
Thompson AM, Gosnell BA, Wagner JJ (Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42:1039-1042.2002).
Toide K, Arima T (Effects of cholinergic drugs on extracellular levels of acetylcholine and choline in rat cortex, hippocampus and striatum studied by brain dialysis. Eur J Pharmacol 173:133-141.1989).
Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H (Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A.2009).
Trujillo KA, Akil H (Opiate tolerance and dependence:recent findings and synthesis. New Biol 3:915-923.1991).
Vanderwolf CH (Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.1969).
Vertes RP (Hippocampal theta rhythm:a tag for short-term memory. Hippocampus 15:923-935.2005).
Vetulani J (Drug addiction. Part II. Neurobiology of addiction. Pol J Pharmacol 53:303-317.2001).
Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL (Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-1178.2001).
Way EL, Loh HH, Shen FH (Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 167:1-8.1969).
White NM (Addictive drugs as reinforcers:multiple partial actions on memory systems. Addiction 91:921-949; discussion 951-965.1996).
Williams S, Johnston D (Long-term potentiation of hippocampal mossy fiber synapses is blocked by postsynaptic injection of calcium chelators. Neuron 3:583-588.1989).
Wolf ME, Mangiavacchi S, Sun X (Mechanisms by which dopamine receptors may influence synaptic plasticity. Ann N Y Acad Sci 1003:241-249.2003).
Woolverton WL, Johnson KM (Neurobiology of cocaine abuse. Trends Pharmacol Sci 13:193-200.1992).
Yang TT, Hung CF, Lee YJ, Su MJ, Wang SJ (Morphine inhibits glutamate exocytosis from rat cerebral cortex nerve terminals (synaptosomes) by reducing Ca2+influx. Synapse 51:83-90.2004).
Zhong W, Dong Z, Tian M, Cao J, Xu T, Xu L, Luo J (Opiate withdrawal induces dynamic expressions of AMPA receptors and its regulatory molecule CaMKIIalpha in hippocampal synapses. Life Sci 79:861-869.2006a).
Zhong WX, Dong ZF, Tian M, Cao J, Xu L, Luo JH (N-methyl-D-aspartate receptor-dependent long-term potentiation in CA1 region affects synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. Neuroscience 141:1399-1413.2006b).
Bauer M, Oostenveld R, Peeters M, Fries P (Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490-501.2006).
Berke JD, Hyman SE (Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.2000).
Bliss TV, Collingridge GL (A synaptic model of memory:long-term potentiation in the hippocampus. Nature 361:31-39.1993).
Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.1995).
Bridger WH, Schiff SR, Cooper SS, Paredes W, Barr GA (Classical conditioning of cocaine's stimulatory effects. Psychopharmacol Bull 18:210-214.1982).
Buzsaki G (Theta oscillations in the hippocampus. Neuron 33:325-340.2002).
Buzsaki G, Eidelberg E (Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 266:334-339.1983).
Chrobak JJ, Buzsaki G (Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.1998).
Csicsvari J, Jamieson B, Wise KD, Buzsaki G (Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.2003).
del Olmo N, Miguens M, Higuera-Matas A, Torres I, Garcia-Lecumberri C, Solis JM, Ambrosio E (Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116:120-126.2006).
Dong Z, Han H, Wang M, Xu L, Hao W, Cao J (Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens. Hippocampus 16:809-813.2006a).
Dong Z, Zhong W, Tian M, Han H, Cao J, Xu T, Luo J, Xu L (Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo. Hippocampus 16:1017-1025.2006b).
Dragoi G, Buzsaki G (Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145-157.2006).
Eisch AJ, Harburg GC (Opiates, psychostimulants, and adult hippocampal neurogenesis: Insights for addiction and stem cell biology. Hippocampus 16:271-286.2006).
Everitt BJ, Robbins TW (Neural systems of reinforcement for drug addiction:from actions to habits to compulsion. Nat Neurosci 8:1481-1489.2005).
Fell J, Fernandez G, Elger CE (More than synchrony:EEG chaoticity may be necessary for conscious brain functioning. Med Hypotheses 61:158-160.2003).
Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.2001).
Fisher NI (Statistical Analysis of Circular Data. Cambridge University Press.1993).
Fries P, Neuenschwander S, Engel AK, Goebel R, Singer W (Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4:194-200.2001).
Gasbarri A, Packard MG, Campana E, Pacitti C (Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445-452.1994).
Gasbarri A, Sulli A, Packard MG (The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22.1997).
Hasselmo ME, Eichenbaum H (Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 18:1172-1190.2005).
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689-707.2002).
Holscher C (Long-term potentiation:a good model for learning and memory? Prog Neuropsychopharmacol Biol Psychiatry 21:47-68.1997).
Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, Schulze-Bonhage A, Kahana MJ (Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369-1374.2003).
Huang YY, Kandel ER (D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446-2450.1995).
Huerta PT, Lisman JE (Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.1993).
Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731.2003).
Hyman SE (Addiction:a disease of learning and memory. Am J Psychiatry 162:1414-1422.2005).
Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28:5959-5964.2008).
Jacobs J, Kahana MJ, Ekstrom AD, Fried I (Brain oscillations control timing of single-neuron activity in humans. J Neurosci 27:3839-3844.2007).
Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N (Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340-348.2008).
Jouvet M (Biogenic amines and the states of sleep. Science 163:32-41.1969).
Karami M, Zarrindast MR, Sepehri H, Sahraei H (Role of nitric oxide in the rat hippocampal CA1 area on morphine-induced conditioned place preference. Eur J Pharmacol 449:113-119.2002).
Kelley AE (Memory and addiction:shared neural circuitry and molecular mechanisms. Neuron 44:161-179.2004).
Lee H, Simpson GV, Logothetis NK, Rainer G (Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45:147-156.2005).
Leung LS (Fast (beta) rhythms in the hippocampus:a review. Hippocampus 2:93-98.1992).
Lisman JE, Idiart MA (Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267:1512-1515.1995).
Lu L, Zeng S, Liu D, Ceng X (Inhibition of the amygdala and hippocampal calcium/calmodulin-dependent protein kinase II attenuates the dependence and relapse to morphine differently in rats. Neurosci Lett 291:191-195.2000).
Malenka RC, Nicoll RA (Long-term potentiation—a decade of progress? Science 285:1870-1874.1999).
Martin PD, Shapiro ML (Disparate effects of long-term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats. Hippocampus 10:207-212.2000).
Masuoka T, Fujii Y, Kamei C (Participation of the hippocampal theta rhythm in memory formation for an eight-arm radial maze task in rats. Brain Res 1103:159-163.2006).
Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (Elements of a neurobiological theory of the hippocampus:the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.2003).
Nestler EJ (Neurobiology. Total recall-the memory of addiction. Science 292:2266-2267.2001).
O'Keefe J, Recce ML (Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.1993).
Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523-7531.2006).
Otmakhova NA, Lisman JE (D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.1996).
Panlilio LV, Schindler CW (Conditioned locomotor-activating and reinforcing effects of discrete stimuli paired with intraperitoneal cocaine. Behav Pharmacol 8:691-698.1997).
Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-1327.2008).
Penttonen M, Kamondi A, Acsady L, Buzsaki G (Gamma frequency oscillation in the hippocampus of the rat:intracellular analysis in vivo. Eur J Neurosci 10:718-728.1998).
Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811.2002).
Pu L, Bao GB, Xu NJ, Ma L, Pei G (Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914-1921.2002).
Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (Gating of human theta oscillations by a working memory task. J Neurosci 21:3175-3183.2001).
Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani A (Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 17:415-423.2003).
Robbins TW, Ersche KD, Everitt BJ (Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1-21.2008).
Robbins TW, Everitt BJ (Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:625-636.2002).
Salinas E, Sejnowski TJ (Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539-550.2001).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Dependence on morphine impairs the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Brain Res 965:108-113.2003a).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Long-term potentiation as an electrophysiological assay for morphine dependence and withdrawal in rats:an in vitro study. J Neurosci Methods 124:189-196.2003b).
Sato N, Yamaguchi Y (Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18:419-424.2007).
Siapas AG, Lubenov EV, Wilson MA (Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.2005).
Skaggs WE, McNaughton BL (Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.1996).
Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.1996).
Stevens KE, Shiotsu G, Stein L (Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region. Brain Res 545:8-16.1991).
Tallon-Baudry C, Bertrand O, Henaff MA, Isnard J, Fischer C (Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 15:654-662.2005).
Thompson AM, Gosnell BA, Wagner JJ (Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42:1039-1042.2002).
Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H (Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad SciU S A.2009).
Vanderwolf CH (Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.1969).
Vetulani J (Drug addiction. Part II. Neurobiology of addiction. Pol J Pharmacol 53:303-317.2001).
Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL (Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-1178.2001).
Way EL, Loh HH, Shen FH (Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 167:1-8.1969).
White NM (Addictive drugs as reinforcers:multiple partial actions on memory systems. Addiction 91:921-949; discussion 951-965.1996).
Woolverton WL, Johnson KM (Neurobiology of cocaine abuse. Trends Pharmacol Sci 13:193-200.1992).
Zhong WX, Dong ZF, Tian M, Cao J, Xu L, Luo JH (N-methyl-D-aspartate receptor-dependent long-term potentiation in CA1 region affects synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. Neuroscience 141:1399-1413.2006).
Amaral DL (ed.) (2006) The Hippocampus Book:Oxford University Press.
Axmacher N, Haupt S, Fernandez G, Elger CE, Fell J (The role of sleep in declarative memory consolidation-direct evidence by intracranial EEG Cereb Cortex 18:500-507.2008).
Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A 107:3228-3233).
Bauer M, Oostenveld R, Peeters M, Fries P (Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490-501.2006).
Bennett TL, Hebert PN, Moss DE (Hippocampal theta activity and the attention component of discrimination learning. Behav Biol 8:173-181.1973).
Bergson C, Levenson R, Goldman-Rakic PS, Lidow MS (Dopamine receptor-interacting proteins: the Ca(2+) connection in dopamine signaling. Trends Pharmacol Sci 24:486-492.2003).
Berke JD, Hyman SE (Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.2000).
Best PJ, White AM (Placing hippocampal single-unit studies in a historical context. Hippocampus 9:346-351.1999).
Biala G, Betancur C, Mansuy 1M, Giros B (The reinforcing effects of chronic D-amphetamine and morphine are impaired in a line of memory-deficient mice overexpressing calcineurin. Eur J Neurosci 21:3089-3096.2005).
Black YD, Green-Jordan K, Eichenbaum HB, Kantak KM (Hippocampal memory system function and the regulation of cocaine self-administration behavior in rats. Behav Brain Res 151:225-238.2004).
Bliss TV, Collingridge GL (A synaptic model of memory:long-term potentiation in the hippocampus. Nature 361:31-39.1993).
Boyer P, Phillips JL, Rousseau FL, Ilivitsky S (Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res Rev 54:92-112.2007).
Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.1995).
Brankack J, Stewart M, Fox SE (Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310-327.1993).
Brazell MP, Mitchell SN, Gray JA (Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats:a dose-response and antagonist study. Neuropharmacology 30:823-833.1991).
Breese CR, Hampson RE, Deadwyler SA (Hippocampal place cells:stereotypy and plasticity. J Neurosci 9:1097-1111.1989).
Bridger WH, Schiff SR, Cooper SS, Paredes W, Barr GA (Classical conditioning of cocaine's stimulatory effects. Psychopharmacol Bull 18:210-214.1982).
Burke SN, Barnes CA (Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30-40.2006).
Buzsaki G (Theta oscillations in the hippocampus. Neuron 33:325-340.2002).
Buzsaki G (2006) Rhythms of the Brain:Oxford University Press.
Buzsaki G, Eidelberg E (Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 266:334-339.1983).
Buzsaki G, Laszlovszky I, Lajtha A, Vadasz C (Spike-and-wave neocortical patterns in rats:genetic and aminergic control. Neuroscience 38:323-333.1990).
Castro NG, de Mello MC, de Mello FG, Aracava Y (Direct inhibition of the N-methyl-D-aspartate receptor channel by dopamine and (+)-SKF38393. Br J Pharmacol 126:1847-1855.1999).
Chao SZ, Ariano MA, Peterson DA, Wolf ME (Dl dopamine receptor stimulation increases GluRl surface expression in nucleus accumbens neurons. J Neurochem 83:704-712.2002a).
Chao SZ, Lu W, Lee HK, Huganir RL, Wolf ME (D(1) dopamine receptor stimulation increases GluRl phosphorylation in postnatal nucleus accumbens cultures. J Neurochem 81:984-992.2002b).
Chrobak JJ, Buzsaki G (Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.1998).
Csicsvari J, Jamieson B, Wise KD, Buzsaki G (Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.2003).
Davidson TL, Jarrard LE (A role for hippocampus in the utilization of hunger signals. Behav Neural Biol 59:167-171.1993).
Deadwyler SA, West M, Lynch G (Activity of dentate granule cells during learning:differentiation of perforant path input. Brain Res 169:29-43.1979).
del Olmo N, Miguens M, Higuera-Matas A, Torres I, Garcia-Lecumberri C, Solis JM, Ambrosio E (Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 1116:120-126.2006).
Diana RA, Yonelinas AP, Ranganath C (Imaging recollection and familiarity in the medial temporal lobe:a three-component model. Trends Cogn Sci 11:379-386.2007).
Dong Z, Han H, Wang M, Xu L, Hao W, Cao J (Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens. Hippocampus 16:809-813.2006a).
Dong Z, Zhong W, Tian M, Han H, Cao J, Xu T, Luo J, Xu L (Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo. Hippocampus 16:1017-1025.2006b).
Dragoi G, Buzsaki G (Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145-157.2006).
Eichenbaum H, Yonelinas AP, Ranganath C (The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123-152.2007).
Eisch AJ, Harburg GC (Opiates, psychostimulants, and adult hippocampal neurogenesis:Insights for addiction and stem cell biology. Hippocampus 16:271-286.2006).
Ekstrom A, Viskontas I, Kahana M, Jacobs J, Upchurch K, Bookheimer S, Fried I (Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus 17:606-617.2007).
Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (Cellular networks underlying human spatial navigation. Nature 425:184-188.2003).
Everitt BJ, Robbins TW (Neural systems of reinforcement for drug addiction:from actions to habits to compulsion. Nat Neurosci 8:1481-1489.2005).
Fell J, Fernandez G, Elger CE (More than synchrony:EEG chaoticity may be necessary for conscious brain functioning. Med Hypotheses 61:158-160.2003).
Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.2001).
Fenton AA, Muller RU (Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U S A 95:3182-3187.1998).
Fiorentini C, Rizzetti MC, Busi C, Bontempi S, Collo G, Spano P, Missale C (Loss of synaptic D1 dopamine/N-methyl-D-aspartate glutamate receptor complexes in L-DOPA-induced dyskinesia in the rat. Mol Pharmacol 69:805-812.2006).
Fisher NI (Statistical Analysis of Circular Data. Cambridge University Press.1993).
Floresco SB, Blaha CD, Yang CR, Phillips AG (Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine:cellular mechanisms of input selection. J Neurosci 21:2851-2860.2001).
Freund RK, Luntz-Leybman V, Collins AC (Nicotine interferes with GABA-mediated inhibitory processes in mouse hippocampus. Brain Res 527:286-291.1990).
Fries P, Neuenschwander S, Engel AK, Goebel R, Singer W (Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4:194-200.2001).
Fukuda M, Kobayashi T, Bures J, Ono T (Rat exploratory behavior controlled by intracranial self-stimulation improves the study of place cell activity. J Neurosci Methods 44:121-131.1992).
Gasbarri A, Packard MG, Campana E, Pacitti C (Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445-452.1994a).
Gasbarri A, Sulli A, Packard MG (The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1-22.1997).
Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat:a combined retrograde tracing and immunohistochemical study. Brain Res 668:71-79.1994b).
Grace AA, Moore H, O'Donnell P (The modulation of corticoaccumbens transmission by limbic afferents and dopamine:a model for the pathophysiology of schizophrenia. Adv Pharmacol 42:721-724.1998).
Hallett PJ, Spoelgen R, Hyman BT, Standaert DG, Dunah AW (Dopamine Dl activation potentiates striatal NMDA receptors by tyrosine phosphorylation-dependent subunit trafficking. J Neurosci 26:4690-4700.2006).
Hasselmo ME, Eichenbaum H (Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 18:1172-1190.2005).
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689-707.2002).
Hirsh R, Davis RE, Holt L (Fornix—thalamus fibers, motivational states, and contextual retrieval. Exp Neurol 65:373-390.1979).
Hirsh R, Holt L, Mosseri A (Hippocampal mossy fibers, motivational states, and contextual retrieval. Exp Neurol 62:68-79.1978a).
Hirsh R, Leber B, Gillman K (Fornix fibers and motivational states as controllers of behavior:a study stimulated by the contextual retrieval theory.Behav Biol 22:463-478.1978b).
Holscher C (Long-term potentiation:a good model for learning and memory? Prog Neuropsychopharmacol Biol Psychiatry 21:47-68.1997).
Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, Schulze-Bonhage A, Kahana MJ (Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369-1374.2003).
Huang YY, Kandel ER (D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446-2450.1995).
Huang YY, Kandel ER, Varshavsky L, Brandon EP, Qi M, Idzerda RL, McKnight GS, Bourtchouladze R (A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83:1211-1222.1995).
Huerta PT, Lisman JE (Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.1993).
Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731.2003).
Hyman SE (Addiction:a disease of learning and memory. Am J Psychiatry 162:1414-1422.2005).
Imperato A, Obinu MC, Gessa GL (Effects of cocaine and amphetamine on acetylcholine release in the hippocampus and caudate nucleus. Eur J Pharmacol 238:377-381.1993).
Ito K, Abekawa T, Koyama T (Valproate blocks high-dose methamphetamine-induced behavioral cross-sensitization to locomotion-inducing effect of dizocilpine (MK-801), but not methamphetamine. Psychopharmacology (Berl) 186:525-533.2006).
Itskov V, Pastalkova E, Mizuseki K, Buzsaki G, Harris KD (Theta-mediated dynamics of spatial information in hippocampus. J Neurosci 28:5959-5964.2008).
Izquierdo I, da Cunha C, Rosat R, Jerusalinsky D, Ferreira MB, Medina JH (Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav Neural Biol 58:16-26.1992).
Jacobs J, Hwang G, Curran T, Kahana MJ (EEG oscillations and recognition memory:theta correlates of memory retrieval and decision making. Neuroimage 32:978-987.2006).
Jacobs J, Kahana MJ, Ekstrom AD, Fried I (Brain oscillations control timing of single-neuron activity in humans. J Neurosci 27:3839-3844.2007).
Jacobs LF (The evolution of the cognitive map. Brain Behav Evol 62:128-139.2003).
Jay TM (Dopamine:a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69:375-390.2003).
Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N (Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340-348.2008).
Jouvet M (Biogenic amines and the states of sleep. Science 163:32-41.1969).
Kaphzan H, O'Riordan KJ, Mangan KP, Levenson JM, Rosenblum K (NMDA and dopamine converge on the NMDA-receptor to induce ERK activation and synaptic depression in mature hippocampus. PLoS One 1:el38.2006).
Karami M, Zarrindast MR, Sepehri H, Sahraei H (Role of nitric oxide in the rat hippocampal CA1 area on morphine-induced conditioned place preference. Eur J Pharmacol 449:113-119.2002).
Kelley AE (Memory and addiction:shared neural circuitry and molecular mechanisms. Neuron 44:161-179.2004).
Kelly C, McCreadie RG (Smoking habits, current symptoms, and premorbid characteristics of schizophrenic patients in Nithsdale, Scotland. Am J Psychiatry 156:1751-1757.1999).
Knierim JJ, McNaughton BL (Hippocampal place-cell firing during movement in three-dimensional space. J Neurophysiol 85:105-116.2001).
Lavenex P, Amaral DG (Hippocampal-neocortical interaction:a hierarchy of associativity. Hippocampus 10:420-430.2000).
Lee FJ, Xue S, Pei L, Vukusic B, Chery N, Wang Y, Wang YT, Niznik HB, Yu XM, Liu F (Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine Dl receptor. Cell 111:219-230.2002).
Lee H, Simpson GV, Logothetis NK, Rainer G (Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45:147-156.2005).
Leung LS (Fast (beta) rhythms in the hippocampus:a review. Hippocampus 2:93-98.1992).
Liang D, Shi X, Qiao Y, Angst MS, Yeomans DC, Clark JD (Chronic morphine administration enhances nociceptive sensitivity and local cytokine production after incision. Mol Pain 4:7.2008).
Linseman MA, Corrigall WA (Effects of morphine on CA1 versus dentate hippocampal field potentials following systemic administration in freely-moving rats. Neuropharmacology 21:361-366.1982).
Lisman JE, Grace AA (The hippocampal-VTA loop:controlling the entry of information into long-term memory. Neuron 46:703-713.2005).
Lisman JE, Idiart MA (Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267:1512-1515.1995).
Liu Y, Sun QA, Chen Q, Lee TH, Huang Y, Wetsel WC, Michelotti GA, Sullenger BA, Zhang X (Targeting inhibition of GluRl Ser845 phosphorylation with an RNA aptamer that blocks AMPA receptor trafficking. J Neurochem 108:147-157.2009).
Lu L, Zeng S, Liu D, Ceng X (Inhibition of the amygdala and hippocampal calcium/calmodulin-dependent protein kinase II attenuates the dependence and relapse to morphine differently in rats. Neurosci Lett 291:191-195.2000).
Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD (Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A97:4398-4403.2000).
Maldonado R, Blendy JA, Tzavara E, Gass P, Roques BP, Hanoune J, Schutz G (Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273:657-659.1996).
Malenka RC, Nicoll RA (Long-term potentiation-a decade of progress? Science 285:1870-1874.1999).
Martin PD, Shapiro ML (Disparate effects of long-term potentiation on evoked potentials and single CA1 neurons in the hippocampus of anesthetized rats. Hippocampus 10:207-212.2000).
Masuoka T, Fujii Y, Kamei C (Participation of the hippocampal theta rhythm in memory formation for an eight-arm radial maze task in rats. Brain Res 1103:159-163.2006).
Meyers RA, Zavala AR, Neisewander JL (Dorsal, but not ventral, hippocampal lesions disrupt cocaine place conditioning. Neuroreport 14:2127-2131.2003).
Meyers RA, Zavala AR, Speer CM, Neisewander JL (Dorsal hippocampus inhibition disrupts acquisition and expression, but not consolidation, of cocaine conditioned place preference. Behav Neurosci 120:401-412.2006).
Mitchell SN, Brazell MP, Joseph MH, Alavijeh MS, Gray JA (Regionally specific effects of acute and chronic nicotine on rates of catecholamine and 5-hydroxytryptamine synthesis in rat brain. Eur J Pharmacol 167:311-322.1989).
Mizuki Y, Tanaka M, Isozaki H, Nishijima H, Inanaga K (Periodic appearance of theta rhythm in the frontal midline area during performance of a mental task. Electroencephalogr Clin Neurophysiol 49:345-351.1980).
Morris RG, Garrud P, Rawlins JN, O'Keefe J (Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.1982).
Morris RG, Moser El, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (Elements of a neurobiological theory of the hippocampus:the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.2003).
Moser MB, Moser El (Functional differentiation in the hippocampus. Hippocampus 8:608-619.1998).
Nestler EJ (Neurobiology. Total recall-the memory of addiction. Science 292:2266-2267.2001).
O'Carroll CM, Morris RG (Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47:324-332.2004).
O'Keefe J, Recce ML (Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.1993).
Ohno M, Shibata S, Yamamoto T, Watanabe S (Working memory deficits following muscarinic blockade combined with depletion of brain somatostatin in rats. Brain Res 610:348-353.1993).
Osipova D, Takashima A, Oostenveld R, Fernandez G, Maris E, Jensen O (Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26:7523-7531.2006).
Otmakhova NA, Lisman JE (D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.1996).
Panlilio LV, Schindler CW (Conditioned locomotor-activating and reinforcing effects of discrete stimuli paired with intraperitoneal cocaine. Behav Pharmacol 8:691-698.1997).
Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-1327.2008).
Pennartz CM, Groenewegen HJ, Lopes da Silva FH (The nucleus accumbens as a complex of functionally distinct neuronal ensembles:an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719-761.1994).
Penttonen M, Kamondi A, Acsady L, Buzsaki G (Gamma frequency oscillation in the hippocampus of the rat:intracellular analysis in vivo. Eur J Neurosci 10:718-728.1998).
Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811.2002).
Pu L, Bao GB, Xu NJ, Ma L, Pei G (Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22:1914-1921.2002).
Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (Gating of human theta oscillations by a working memory task. J Neurosci 21:3175-3183.2001).
Rector DM, Poe GR, Harper RM (Imaging of hippocampal and neocortical neural activity following intravenous cocaine administration in freely behaving cats. Neuroscience 54:633-641.1993).
Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani A (Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 17:415-423.2003).
Ridley RM, Aitken DM, Baker HF (Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus. Brain Res 502:306-318.1989).
Robbins TW, Ersche KD, Everitt BJ (Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141:1-21.2008).
Robbins TW, Everitt BJ (Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:625-636.2002).
Salinas E, Sejnowski TJ (Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539-550.2001).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Dependence on morphine impairs the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Brain Res 965:108-113.2003a).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M (Long-term potentiation as an electrophysiological assay for morphine dependence and withdrawal in rats:an in vitro study. J Neurosci Methods 124:189-196.2003b).
Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M, Kazemnejad A (Dependence on morphine leads to a prominent sharing among the different mechanisms of long-term potentiation in the CA1 region of rat hippocampus. Brain Res 963:93-100.2003c).
Sato N, Yamaguchi Y (Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18:419-424.2007).
Schridde U, van Luijtelaar G (The role of hippocampal theta activity in sensory gating in the rat. Physiol Behav 74:257-266.2001).
Scoville WB, Milner B (Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.1957).
Seamans JK, Yang CR (The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58.2004).
Sharp PE, McNaughton BL, Barnes CA (Enhancement of hippocampal field potentials in rats exposed to a novel, complex environment. Brain Res 339:361-365.1985).
Siapas AG, Lubenov EV, Wilson MA (Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.2005).
Silverstone PH, Done C, Sharp T (In vivo monoamine release during naloxone-precipitated morphine withdrawal. Neuroreport 4:1043-1045.1993).
Skaggs WE, McNaughton BL (Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.1996).
Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.1996).
Spielewoy C, Gonon F, Roubert C, Fauchey V, Jaber M, Caron MG, Roques BP, Hamon M, Betancur C, Maldonado R, Giros B (Increased rewarding properties of morphine in dopamine-transporter knockout mice. Eur J Neurosci 12:1827-1837.2000).
Stevens KE, Shiotsu G, Stein L (Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region. Brain Res 545:8-16.1991).
Sutherland GR, McNaughton B (Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180-186.2000).
Tallon-Baudry C, Bertrand O, Henaff MA, Isnard J, Fischer C (Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 15:654-662.2005).
Thompson AM, Gosnell BA, Wagner JJ (Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42:1039-1042.2002).
Toide K, Arima T (Effects of cholinergic drugs on extracellular levels of acetylcholine and choline in rat cortex, hippocampus and striatum studied by brain dialysis. Eur J Pharmacol 173:133-141.1989).
Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H (Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A.2009).
Trujillo KA, Akil H (Opiate tolerance and dependence:recent findings and synthesis. New Biol 3:915-923.1991).
Vanderwolf CH (Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.1969).
Vertes RP (Hippocampal theta rhythm:a tag for short-term memory. Hippocampus 15:923-935.2005).
Vetulani J (Drug addiction. Part II. Neurobiology of addiction. Pol J Pharmacol 53:303-317.2001).
Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL (Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-1178.2001).
Way EL, Loh HH, Shen FH (Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 167:1-8.1969).
White NM (Addictive drugs as reinforcers:multiple partial actions on memory systems. Addiction 91:921-949; discussion 951-965.1996).
Williams S, Johnston D (Long-term potentiation of hippocampal mossy fiber synapses is blocked by postsynaptic injection of calcium chelators. Neuron 3:583-588.1989).
Wolf ME, Mangiavacchi S, Sun X (Mechanisms by which dopamine receptors may influence synaptic plasticity. Ann N Y Acad Sci 1003:241-249.2003).
Woolverton WL, Johnson KM (Neurobiology of cocaine abuse. Trends Pharmacol Sci 13:193-200.1992).
Yang TT, Hung CF, Lee YJ, Su MJ, Wang SJ (Morphine inhibits glutamate exocytosis from rat cerebral cortex nerve terminals (synaptosomes) by reducing Ca2+influx. Synapse 51:83-90.2004).
Zhong W, Dong Z, Tian M, Cao J, Xu T, Xu L, Luo J (Opiate withdrawal induces dynamic expressions of AMPA receptors and its regulatory molecule CaMKIIalpha in hippocampal synapses. Life Sci 79:861-869.2006a).
Zhong WX, Dong ZF, Tian M, Cao J, Xu L, Luo JH (N-methyl-D-aspartate receptor-dependent long-term potentiation in CA1 region affects synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. Neuroscience 141:1399-1413.2006b).