1 Neurobiologie des Processus Adaptatifs, Université Paris VI, France, 2 Laboratoire de Signalisation Cellulaire et Parasites, Hôpital Cochin, Paris, France
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Dopamine Modulates Glutamatergic Transmission in the Prefrontal Cortex |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Modulation of PFC glutamatergic transmission by dopamine has been studied at the cellular level. For example, it was shown that at least D1 subtype of dopamine receptors co-localize with glutamate receptors on dendritic spines and shafts of pyramidal neurons in monkey frontal layers II and V (Smiley et al., 1994; Bergson et al., 1995
). Electrophysiologically, the D1 agonist was shown to reduce excitatory transmission in collateral synapses between a pair of layer V pyramidal neurons (Gao et al., 2001
). Pyramidal neuron collateral transmission is believed to participate in the generation of the sustained delay period activity (Goldman-Rakic, 1995
). Interestingly, collateral transmission between layer III pyramidal neurons in monkey PFC slices was unaffected by dopamine (Urban et al., 2002
), while dopamine reduced excitatory transmission in the presumably projection fiber synapses on the same neurons (Urban et al., 2002
). In rat PFC slices, dopamine inhibits glutamatergic transmission at layer V pyramidal neurons after stimulation of the superficial (Law-Tho et al., 1994
, 1995; Otani et al., 1998
, 1999) or deep layer fibers (Law-Tho et al., 1994
). The deep layer afferents probably contain projection fibers from the hippocampus (Jay and Witter, 1991
), which is involved in working memory (Floresco et al., 1997
) and schizophrenia pathogenesis (Lipska and Weinberger, 2002
). Several in vivo studies confirm that the synaptic transmission in the hippocampo-PFC monosynaptic connection is inhibited by dopamine (Jay et al., 1995b
; Gurden et al., 1999
; Floresco and Grace, 2003
).
![]() |
Lasting Neural Traces in the PFC |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Long-term Synaptic Plasticity in Rat PFC Neurons |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Pioneering in vitro studies on LTP and LTD in rat PFC (Hirsch and Crepel, 1990, 1991, 1992) showed that the application of 50 or 100 Hz tetanic stimuli to layer I-II afferent fibers in the presence of
-aminobutyric acid A (GABA-A) antagonist bicuculline induce LTP or LTD of monosynaptic glutamatergic responses in the portion of layer V pyramidal neurons. Both LTP and LTD are dependent on postsynaptic Ca2+ increases (Hirsch and Crepel, 1992
). For LTP, but not LTD, at least part of the critical Ca2+ enter through NMDA (N-methyl-D-aspartate) receptor-linked ion channels, because the NMDA receptor antagonist AP5 (DL-2-amino-5-phosphonopentanoic acid) selectively blocks LTP and unmasks underlying LTD (Hirsch and Crepel, 1991
).
NMDA receptor-dependency of LTP was also shown by Vickery et al. (1997) in the identical preparation. In this case, they applied stimuli mimicking hippocampal theta burst (four shocks at 100 Hz, repeated 10 times in every 200 ms) and showed LTP induction in
60% of the neurons tested. AP5 significantly reduced this LTP. It is known that in hippocampal neurons, the short burst (four shocks) primes the stimulated dendrites so that a successive burst arriving 200 ms later optimally activates the voltage-dependent NMDA receptor-channel complex (Larson and Lynch, 1988
). Thus, the 10 times repetitive applications of the burst (Vickery et al., 1997
) should strongly activate NMDA receptors to induce LTP.
Anatomically, there is a monosynaptic projection from ventral CA1/subiculum to the prelimbic area in the rat (Jay and Witter, 1991). Therefore, theta-patterned discharge of hippocampal neurons may excite prelimbic synapses to induce NMDA-dependent LTP under, for example, exploratory behavioral conditions (O'Keefe and Nadel, 1978
). Although the effect of theta burst stimuli to the hippocampo-PFC synapses has not been tested, LTP in this connection was induced by brief 250 Hz tetanic stimuli (Laroche et al., 1990
), and it was shown to be NMDA-dependent (Jay et al., 1995a
).
Dopaminergic Facilitation of Prefrontal LTD
As discussed above, application of tetanic stimuli (50 or 100 Hz) induced LTP or LTD in the layer I-II to layer V pyramidal neuron glutamatergic synapses in rat PFC slices (Hirsch and Crepel, 1990, 1991, 1992). Law-Tho et al. (1995)
found that the presence of dopamine (50100 µM) in the bathing medium during tetanic stimuli facilitates LTD and inhibits LTP. Dopamine application alone only transiently depressed the synaptic responses. Subsequent studies (Otani et al., 1998
, 1999) fixed the train parameter as 50 Hz, 2 s (four times at 0.1 Hz), and showed that while the tetanic stimuli alone do not induce lasting plasticity, application of the stimuli in the presence of dopamine consistently induces LTD (Fig. 1). Dopamine acts through both D1 and D2 dopamine receptors for the induction of this LTD (Otani et al., 1998
). The dopamine-facilitated LTD does not require NMDA receptors but requires postsynaptic depolarization and postsynaptic Ca2+ increases (Otani et al., 1998
), consistent with the earlier studies (Hirsch and Crepel, 1991
, 1992).
|
Enhancement of Postsynaptic Excitability by Dopamine
It was shown that dopamine enhances late postsynaptic depolarization during the LTD-inducing 50 Hz stimuli while it reduces postsynaptic responses evoked by low-frequency stimuli (Otani et al., 1998; Otani and Kolomiets, 2003
). Dopamine also increases the number of spikes upon depolarizing current injection (Penit-Soria et al., 1987
; Yang and Seamans, 1996
) through D1 receptor activation (Yang and Seamans, 1996
). Underlying mechanisms of this effect may be the enhancement of tetrodotoxin-sensitive slowly-inactivating persistent Na+ current (INaP) and the attenuation of slowly inactivating, outwardly rectifying K+ current (Yang and Seamans, 1996
). Dopamine action on the INaP may require protein kinase C (PKC) (Gorelova and Yang, 2000
).
Despite these data, however, it is still unclear whether the enhancement of postsynaptic excitability by dopamine is necessary for LTD induction in deep layer pyramidal neurons of the PFC. First, there are contradictions in the literature. Geijo-Barrientos and Pastore (1995) found a reduction of the INaP by dopamine in layer IIVI regular spiking neurons. Gulledge and Jaffe (1998
) found a reduction in the number of spikes in layer V pyramidal neurons by D2 receptors. Maurice et al. (2001)
found no effect of dopamine on the INaP in acutely dissociated PFC pyramidal neurons. These results are rather consistent to dopamine effects found in striatal medium spiny neurons (Nicola et al., 2000
) (see Concluding Remarks for more discussion). Secondly, more importantly, our recent analysis showed that the dopaminergic enhancement of postsynaptic depolarization during 50 Hz tetanus is blocked by NMDA antagonist AP5 (Otani and Kolomiets, 2003
; see also Wang and O'Donnell, 2001
), but LTD is inducible in the presence of AP5 (Otani et al., 1998
). Thus, the enhancement of depolarization by dopamine during tetanus appears unnecessary for LTD, although it is possible that depolarization enhancement in local dendritic sites was not adequately monitored by somatic electrodes.
But, the NMDA-dependent enhancement of postsynaptic depolarization by dopamine may play roles in online information processing. Recent modeling studies (Durstewitz et al., 2000; Brunel and Wang, 2001
) suggest that an increase in NMDA-mediated conductance by dopamine is a major factor to cause the enhancement of signal-to-noise ratio and the stabilization of sustained high-frequency collateral activity during delay period of working memory tasks.
Cooperativity between Dopamine Receptors and mGluRs
Blockade of group I or group II mGluRs during tetanus blocked dopamine-facilitated LTD (Otani et al., 1999). This result suggests that the dopamine receptors and the groups I and II mGluRs cooperate for LTD induction in the PFC. The following lines of evidence showed that this cooperativity involves postsynaptic converging activation of MAP-Ks (mitogen-activated protein kinases) (Valjent et al., 2001
) by dopamine receptors and the mGluRs (see Fig. 2A). First, LTD could be induced by combined bath-application of dopamine and the group I and II mGluR agonist ACPD [(1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid] (Otani et al., 1999
). Secondly, this LTD was blocked by postsynaptic inhibition of MAP-Ks (Otani et al., 1999
). Thirdly, Western blot analyses with anti-active MAP-Ks antibody showed that MAP-Ks are activated by dopamine, a group I mGluR agonist, and a group II mGluR agonist (Otani et al., 1999
). Fourthly, combined application of dopamine and one of these mGluR agonists synergistically or additively activated MAP-Ks (Otani et al., 1999
). Although critical target(s) of the MAP-Ks for LTD induction is still unknown, a study in the hippocampus suggested a link between MAP-Ks and the modification of dendritic spine shape (Wu et al., 2001
). Also in the hippocampus, MAP-Ks are necessary for the phosphorylation of CREB (cyclic AMP response element-binding protein) by PKC and protein kinase A (PKA) (Roberson et al., 1999
), confirming the importance of the MAP-Ks as a mediator for long-term cellular changes (Valjent et al., 2001
; Fig. 2A).
|
In Vivo Studies
Gurden et al. (1999) tested the effect of VTA stimulation on LTP of the hippocampo-PFC monosynaptic projection (Jay and Witter, 1991
) in anesthetized rats. First, single VTA stimulation just before a test pulse delivery to the ventral CA1/subiculum reversibly depressed the hippocampo-PFC synaptic responses, consistent with the observation made in vitro that bath-applied dopamine transiently depresses PFC synaptic responses (Law-Tho et al., 1995
; Otani et al., 1998
, 1999). Second, application of 50 Hz 2 sec stimuli to the VTA 2 sec before 250 Hz tetanus to the ventral CA1/subculum enhanced LTP induced by the 250 Hz tetanus. Third, VTA lesion reduced the magnitude of LTP induced by the 250 Hz tetanus. Gurden et al. (2000)
subsequently showed that the hippocampal stimulation evokes dopamine release in the PFC. In terms of the mechanism, it was shown that dopamine stimulates PKA through D1 receptors to facilitate LTP (Gurden et al., 2000
). Because LTP in the PFC requires NMDA receptors (Hirsch and Crepel, 1991
; Jay et al., 1995a
), D1 receptors and NMDA receptors may cooperate in LTP-inducing mechanisms (see Fig. 2B). Interestingly, Baldwin et al. (2002)
showed that normal acquisition of appetitive operant conditioning in the rat requires D1 receptors, NMDA receptors, and PKA in the PFC. This agreement at the cellular level supports the idea that LTP-like processes in the PFC may be involved in learning and memory (Herry and Garcia, 2002
; Otani, 2002
).
In vitro Studies
Dopaminergic facilitation of LTP was not seen in the in vitro studies (Law-Tho et al., 1995; Otani et al., 1998
, 1999). A critical difference between the intact brain and the brain slice preparations may be the lack of baseline stimulation of dopamine receptors in the slice preparation. Dopaminergic axons are severed and probably inactive in the slices, because if it is otherwise, the application of dopamine receptor antagonists should augment the synaptic responses. We detect no such effects (unpublished observations). We suggest that during a few-hour pre-conditioning period, dopamine receptors in the PFC slices are largely unstimulated. By contrast, baseline stimulation of dopamine receptors occurs in the physiological situations, since dopamine levels in the PFC are tonically maintained (Takahata and Moghaddam, 2000
) and show repeated increases during behavior (Bassareo and Di Chiara, 1997
).
We attempted to partially control this factor by exposing the slices to bath-applied dopamine first (1015 min; Blond et al., 2002; Fig. 3). When the synaptic responses recovered from the transient inhibitory effect of dopamine (in
30 min), dopamine was identically applied for the second time. This second application was coupled to 50 Hz stimuli. This protocol induced LTP, not LTD (Blond et al., 2002
; Fig. 3). The second application of dopamine was necessary for LTP induction (Blond et al., 2002
).
|
![]() |
Concluding Remarks |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In conclusion, in order to accurately assess short- and long-lasting cellular effects of dopamine in the PFC, anatomical identification of stimulated axons and neurons, and a good control over the application protocol and the pattern of VTA stimulation must be taken into consideration.
![]() |
Notes |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Address correpondence to: Satoru Otani, Neurobiologie des Processus Adaptatifs, UMR7102, Université Paris VI, case8, 7, quai St Bernard, 75005 Paris, France. Email: satoru.otani{at}snv.jussieu.fr.
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Assad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:13991407.[ISI][Medline]
Baldwin AE, Sadeghian K, Kelly AE (2002) Appetitive instumental learning requies coincident activation of NMDA and dopamine D1 receptor within the medial prefrontal cortex. J Neurosci 22:10631071.[CrossRef][ISI][Medline]
Bassareo V, Di Chiara G (1997) Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. J Neurosci 17:851861.
Bergson C, Mrzljak L, Smiley JF, Pappy M, Levenson R, Goldman-Rakic PS (1995) Regional, cellular, and subcellular variations in the distributions of D1 and D5 dopamine receptors in primate brain. J Neurosci 15:78217836.[Abstract]
Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:43204324.
Blond O, Crepel F, Otani S (2002) Long-term potentiation in rat prefrontal slices facilitated by phased application of dopamine Eur J Pharmacol 438:115116.[CrossRef][ISI][Medline]
Brunel N, Wang X-J (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J Comput Neurosci 11:6385.[CrossRef][ISI][Medline]
Christie BR, Abraham WC (1992) Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9:7984.[ISI][Medline]
Durstewitz D, Seamans JK, Sejnowski TJ (2000) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83:17331750.
Floresco SB, Grace AA (2003) Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 23:39303943.
Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:18801890.
Fuster JM (1973) Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 36:6178.
Gao WJ, Krimer LS, Goldman-Rakic PS (2001) Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. Proc Natl Acad Sci USA 98:295300.
Geijo-Barrientos, E and Pastore, C (1995) The effects of dopamine on the subthreshold electrophysiological responses of rat prefrontal cortex neurons in vitro. Eur J Neurosci 7:358366.[ISI][Medline]
Glowinski J, Tassin JP, Thierry AM (1984) The mesocortico-prefrontal dopaminergic neurons. Trends Neurosci 7:415418.
Goldman-Rakic P (1995) Cellular basis of working memory. Neuron 14:477485.[ISI][Medline]
Gorelova NA, Yang CR (2000) Dopamine D1/D5 receptor activation modulates a persistent sodium current in rat prefrontal cortical neurons in vitro. J Neurophysiol 84:7587.
Gulledge AT, Jaffe DB (1998) Dopamine decreases the excitability of layer V pyramidal cells in the rat prefrontal cortex. J Neurosci 18:91399151.
Gulledge AT, Jaffe DB (2001) Multiple effects of dopamine on layer V pyramidal cell excitability in rat prefrontal cortex. J Neurophysiol 86:586595.
Gurden H, Tassin J-P, Jay TM (1999) Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation. Neuroscience 94:10191027.[CrossRef][ISI][Medline]
Gurden H, Takita M, Jay TM (2000) Essential role of D1 but not D2 receptors in the NMDA receptor-dependent long-term potentiation at hippocampal-prefrontal cortex synapses in vivo. J Neurosci 20:RC106.[Medline]
Herry C, Garcia R (2002) Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci 22:577583.
Hirsch JC, Crepel F (1990) Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. J Physiol (Lond) 427:3149.[Abstract]
Hirsch JC, Crepel F (1991) Blockade of NMDA receptors unmasks a long-term depression in synaptic efficacy in rat prefrontal neurons in vitro. Exp Brain Res 85:621624.[ISI][Medline]
Hirsch JC, Crepel F (1992) Postsynaptic calcium is necessary for the induction of LTP and LTD of monosynaptic EPSPs in prefrontal neurons: an in vitro study in the rat. Synapse 10:173175.[ISI][Medline]
Jay TM, Witter MP (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313:574586.[ISI][Medline]
Jay TM, Burette F, Laroche S (1995a) NMDA receptor-dependent LTP in the hippocampal afferent fibre system to the prefrontal cortex in the rat. Eur J Neurosci 7:247250.[ISI][Medline]
Jay TM, Glowinski J, Thierry AM (1995b) Inhibition of hippocampo-prefrontal cortex excitatory responses by the mesocortical DA system. Neuroreport 6:18451848.[ISI][Medline]
Kosobud AE, Glenda CH, Chapin JK (1994) Behavioral associations of neuronal activity in the ventral tegmental area of the rat. J Neurosci 14:71177129.[Abstract]
Laroche S, Jay TM, Thierry A-M (1990) Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci Lett 114:184190.[CrossRef][ISI][Medline]
Larson J, Lynch G (1988) Role of N-methyl-D-aspartate receptors in the induction of synaptic potentiation by burtst stimulation patterned after the hippocampal theta-rhythm. Brain Res 441:111118.[CrossRef][ISI][Medline]
Law-Tho D, Hirsch, JC, Crepel F (1994) Dopamine modulation of synaptic transmission in rat prefrontal cortex: an in vitro electrophysiological study. Neurosci Res 21:151160.[CrossRef][ISI][Medline]
Law-Tho D, Desce JM, Crepel F (1995) Dopamine favours the emergence of long-term depression versus long-term potentiation in slices of rat prefrontal cortex. Neurosci Lett 188:125128.[CrossRef][ISI][Medline]
Lipska BK, Weinberger DR (2002) A neurodevelopmental model of schizophrenia: neonatal disconnection of the hippocampus. Neurotox Res 4:469475.[CrossRef][Medline]
Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145163.
Maurice N, Tkatch T, Meisler M, Sprunger LK, Surmeier DJ (2001) D1/D5 dopamine receptor activation differentially modulates rapidly inactivating and persistent sodium currents in prefrontal cortex pyramidal neurons. J Neurosci 21:22682277.
Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449451.[CrossRef][ISI][Medline]
Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui D-H, Tabira T (2000) Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 15:15681574.
Mulder AB, Nordquist R, Örgüt O, Pennartz CMA (2000) Plasticity of neuronal firing in deep layers of the medial prefrontal cortex in rats engaged in operant conditioning. Prog Brain Res 126:287301.
Nicola SM, Surmeier DJ, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185215.[CrossRef][ISI][Medline]
Nisson CL, Hellstrand M, Ekman A, Eriksson E (1998) Direct dopamine D2-receptor-mediated modulation of arachidonic acid release in transfected CHO cells without the concomitant administration of a Ca2+-mobilizing agent. Br J Pharmacol 124:16511658.[Abstract]
OKeefe J, Nadel L (1978) Hippocampus as a cognitive map. Oxford: Clarendon Press.
Otani S (2002) Memory trace in prefrontal cortex: theory for the cognitive switch. Biol Rev 77:563577.[CrossRef][Medline]
Otani S (2003) Prefrontal cortex function, quasi-physiological stimuli, and synaptic plasticity. J Physiol (Paris) (in press).
Otani S, Kolomiets B (2003) Induction properties of synaptic plasticity in rat prefrontal neurons In: Prefrontal cortex: from synaptic plasticity to cognition (Otani S, ed.). Boston, MA: Kluwer Aademic Publishers (in press).
Otani S, Blond O, Desce J-M, Crepel F (1998) Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex. Neuroscience 85:669676.[CrossRef][ISI][Medline]
Otani S, Auclair N, Desce J-M, Roisin M-P, Crepel F (1999) Dopamine receptors and groups I & II mGluRs cooperate for LTD induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases. J Neurosci 19:97889802.
Otani S, Daniel H, Takita M, Crepel F (2002) Long-term depression induced by postsynaptic group II mGluRs linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci 22:34343444.
Penit-Soria J, Audinat E, Crepel F (1987) Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiological study. Brain Res 42:263274.[CrossRef]
Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD (1999) The mitogen-activated protein kinae cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19:43374348.
Rossi S, Cappa SF, Babiloni C, Pasqualetti P, Miniussi C, F Carducci, Babiloni F, Rossini PM (2001) Prefrontal cortex in long-term memory: an interference approach using magnetic stimulation. Nat Neurosci 4:948952.[CrossRef][ISI][Medline]
Rossi S, Miniussi C, P Rossini M, Babiloni C, Cappa S (2003) Transcranial magnetic stimulation of the prefrontal cortex: a complementary approach to investigate human long-term memory. In: Prefrontal cortex: synaptic plasticity to cognition (Otani S, ed.). Boston, MA: Kluwer Academic Publishers (in press).
Sawaguchi T, Goldman-Rakic PS (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251:947950.[ISI][Medline]
Sawaguchi T, Goldman-Rakic PS (1994) The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 71:515528.
Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900913.[Abstract]
Seamans JK, Durstewitz D, Christie BR, Stevens CF, Sejnowski TJ (2001) Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci USA 98:301306.
Smiley JF, Levey AL, Ciliax BJ, Goldman-Rakic PS (1994) D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci USA 91:57205724.[Abstract]
Takahata R, Moghaddam B (2000) target-specific glutamate regulation of dopamine neurons in the ventral tegmental area. J Neurochem 75:17751778.[CrossRef][ISI][Medline]
Urban NN, Gonzàlez-Burgos G, Henze DA, Lewis DA, Barrionuevo G (2002) Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex. J Physiol (Lond) 539:707712.
Valjent E, Caboche J, Vanhoutte P (2001) Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain. Mol Neurobiol 23:8399.[ISI][Medline]
Vial D, Piomelli D (1995) Dopamine D2 receptors potentiate arachidonate release via activation of cytosolic, arachidonate-specific phospholipase A2. J Neurochem 64:27652772.[ISI][Medline]
Vickery RM, Morris SH, Bindmann LJ (1997) Metabotropic glutamate receptors are involved in long-term potentiation in isolated slices of rat medial frontal cortex. J Neurophysiol 78:30393046.
Wang J, ODonnell P (2001) D1 dopamine receptors potentiate NMDA-mediated excitability increases in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 11:452462.
William GV, Goldman-Rakic PS (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376:612.
Wu G-Y, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4:151158.[CrossRef][ISI][Medline]
Yang CR, Seamans JK (1996) Dopamine D1 receptor actions in layers VVI rat prefrontal cortex neurons in vitro: modulation of dendriticsomatic signal integration. J Neurosci 16:19221935.[Abstract]
Zahrt J, Taylor JR, Mathew RG, Arnsten AFT (1997) Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 17:85288535.