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NEUROPHARMACOLOGY
Department of Pharmaceutical Sciences, North Dakota State University, Fargo, North Dakota (H.H.); and Department of Physiology and Pharmacology, University of Georgia, Athens, Georgia (J.J.W.)
Received June 24, 2005; accepted September 8, 2005.
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Abstract |
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) and investigated using animal models (Chambers and Taylor, 2004). Data obtained from rats utilizing either the neonatal hippocampal lesion (schizophrenia) or self-administration (substance use) animal models have suggested that the hippocampus is likely to be involved in both schizophrenia (Harrison, 2004), and drug relapse (Vorel et al., 2001; Sun and Rebec, 2003). It is therefore important to determine the role of the endogenous dopamine transmitter system in normal and pathological hippocampal function.
The understanding of the actions of dopamine as a neurotransmitter in the hippocampal formation has evolved over the past 3 decades, from the presumption that dopamine had no significant role (except as a precursor to norepinephrine), to the current appreciation that dopamine can act via multiple signaling pathways in the hippocampus. For example, in the CA1 region, potential physiological actions include the modulation of a calcium-activated K+ current (Benardo and Prince, 1982; Pockett, 1985; Malenka and Nicoll, 1986; Berretta et al., 1990; Pedarzani and Storm, 1995), excitatory neurotransmission (Hsu, 1996; Otmakhova and Lisman, 1998; Yang, 2000; Kotecha et al., 2002), voltage-gated ion channels (Cantrell et al., 1997; Hoffman and Johnston, 1999), and inhibitory neurotransmission (Gribkoff and Ashe, 1984a,b). The observations concerning effects on the calcium-activated K+ current and on evoked EPSPs are somewhat controversial because both enhancements and inhibitions of each of these measures by dopamine agonists are reported.
In addition, several reports have also described the effects of dopamine on long-term potentiation (LTP) at the Schaffer collateral synapse in the CA1 region. D1/5 dopamine antagonists inhibit both late LTP (Frey et al., 1991; Swanson-Park et al., 1999) and early LTP (Otmakhova and Lisman, 1996), as well as long-term depression (Chen et al., 1995), suggesting that endogenous dopamine facilitates synaptic plasticity in the CA1 region of the hippocampus. We have reported recently that LTP is significantly enhanced in the presence of the monoamine transporter blockers, and this action is prevented by a dopamine D2-like receptor antagonist (Thompson et al., 2005). Since GABAergic synaptic transmission exerts a powerful influence over LTP induction at Schaffer collateral synapses (Davies et al., 1991), we have tested the hypothesis that dopamine might modulate GABAergic IPSCs in the CA1 region of the hippocampus.
In this report, we show that the application of either cocaine or a selective D3 dopamine receptor agonist can inhibit the monosynaptic IPSCs evoked from stratum radiatum and recorded in CA1 pyramidal neurons and that a selective D3 dopamine receptor antagonist was effective in preventing these actions. Our findings point to a newly appreciated role for the D3 dopamine receptor subtype in mediating a disinhibition in CA1 that can lead to a net excitation of pyramidal neurons in this region of the hippocampus (a preliminary description of this work has appeared previously, Hammad and Wagner, 2004).
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Materials and Methods |
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30 sec in ice-cold, oxygenated (95/5% O2/CO2) artificial cerebrospinal fluid (ACSF; composition: 125 mM NaCl, 3 mM KCl, 1 mM NaH2PO4, 1.5 mM MgCl2, 2.5 mM CaCl2, 26 mM NaHCO3, and 10 mM glucose, pH 7.4), and then 400 or 500 µM sections were cut on a Vibraslice microtome. Hippocampal slices were dissected free, and the CA3 region was surgically removed. The slices were transferred to a holding chamber containing oxygenated ACSF and allowed to recover at room temperature for at least 1 h. The slices were then transferred to a heated, submersion-type recording chamber where they were perfused at a flow rate of 1.5 to 2 ml/min of oxygenated ACSF and warmed to 30°C during an additional recovery hour.
Whole-Cell Electrophysiology. Whole-cell recording electrodes (3–5 M
) were pulled on a Sutter P-97 horizontal micropipette puller using 1.5-mm thin-wall borosilicate glass tubing (WPI, Sarasota, FL). Blind recordings from the pyramidal layer of the CA1 region were done using a motorized micromanipulator with the aid of a dissecting microscope. Passive properties (holding current, input resistance) as well as synaptic currents were monitored in voltage-clamp using an Axopatch 200B amplifier, and the data were acquired and analyzed using pCLAMP 9 software (Molecular Devices, Sunnyvale, CA). A holding potential of –60 mV was used for all recordings. A bipolar stimulating electrode (Kopf Instruments, Tujunga, CA) was connected to constant current stimulus isolation unit (WPI) and used to evoke synaptic currents.
The following intracellular recording solution was used: 145 mM KMeSO3, 2 mM MgCl2, 2 mM EGTA, 0.2 mM CaCl2, 2 mM Mg-ATP, and 2 mM HEPES, pH 7.2, with KOH. Pharmacologically isolated IPSCs were evoked in the presence of 2,3-dihydroxy-6,7-dinitroquinoxaline (10 µM) and 2-amino-5-phosphonovalerate (50 µM). The peak amplitude of this monosynaptic IPSC response was used for comparative analysis (paired Student's t test before/after drug application). Pharmacologically isolated EPSCs were evoked in the presence of picrotoxin (100 µM) and intracellular QX314 (5 mM). The peak amplitude of the EPSC response was used for comparative analysis (paired Student's t test before/after drug application).
Extracellular Electrophysiology. Population spike (PS) responses were measured from recording electrodes placed in the CA1 pyramidal cell body layer following stimulation of the stratum radiatum. The baseline stimulus intensity was set at a level evoking a PS of 40 to 60% of maximal amplitude. A pair of responses (PS1 and PS2) was evoked at an interstimulus interval of 10 ms. For each response, the peak negative amplitude was subtracted from the peak positive amplitude to obtain the amplitudes of PS1 and PS2. The PS2/PS1 ratio was then calculated for a 5-min period both immediately before and 15 to 20 min following drug application. This paired-pulse ratio was used for comparative analysis (paired Student's t test before/after drug application).
Drugs and Chemicals. For drug application, all drugs were applied via bath perfusion, using a three-way valve. The dead volume of the tubing and chamber was <2 ml, allowing rapid onset (<5 min) for most compounds at the typical perfusion rate. Cocaine hydrochloride was obtained from the National Institute on Drug Abuse (RTI, Research Triangle Park, NC), and both PD 128907 and U 99194 maleate were obtained from Tocris Cookson Inc. (Ellisville, MO). All other drugs/chemicals were obtained from Sigma Diagnostics (St. Louis, MO).
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). Those results demonstrate that cocaine at the concentration that we have chosen for the present studies (i.e., 10 µM) acts primarily by blocking monoamine transporters and by the subsequent activation of dopamine receptors. In our experimental preparation, cocaine does not have significant effects as a local anesthetic at concentrations lower than 30 µM (see also Dunwiddie et al., 1988). Thus, we have tested the hypothesis that cocaine inhibited the monosynaptic IPSC by increasing endogenous monoamine transmitter levels and activating dopamine receptors. A series of dopamine receptor antagonists were tested to determine if there is a receptor subtype-selective effect of cocaine on the evoked IPSC. Preincubation (15+ min prior to cocaine application) with the D1/5 antagonist SCH 23390 (3 µM) did not significantly affect the ability of cocaine to inhibit the IPSC (Fig. 2A, 75 ± 2%, n = 7). In contrast, pretreatment with the D2-like antagonist eticlopride (3 µM) completely prevented the inhibitory effects of cocaine on the IPSC (Fig. 2B, 98 ± 7%, n = 5). Attempts to reverse the actions of cocaine with eticlopride application following the 20-min exposure to cocaine were not successful (data not shown). The D2-like dopamine receptor class consists of three subtypes, D2, D3, and D4 receptors. As observed with eticlopride, preincubation with either the potent D2/3 receptor antagonist raclopride (30 nM, Fig. 2C, 96 ± 9%, n = 5) or the D3-selective receptor antagonist U 99194 maleate (1 µM, Fig. 2D, 104 ± 7%, n = 5) prevented the inhibitory effects of cocaine on the IPSC, suggesting that activation of the D3 subtype of dopamine receptor is mediating these effects.
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A D3-Selective Agonist Can Mimic the Effects of Cocaine on the IPSC. To further test the hypothesis that D3 receptors mediate the effects of cocaine, the selective D3 receptor agonist PD 128907 (1 µM) was bath applied to the slice. As was the case with cocaine, PD 128907 had an inhibitory effect on the monosynaptic IPSC amplitude (Fig. 3, A and C, 76 ± 6%, n = 9). The input resistance of these neurons was 97 ± 11 M prior to drug exposure and did not change significantly in the presence of the D3 receptor agonist (108 ± 12 M, p > 0.25). Preincubation with the selective D3 receptor antagonist U 99194 (1 µM, Fig. 3, B and C, 91 ± 7%, n = 7) prevented any significant inhibition of the IPSC amplitude by PD 128907. Thus, both in terms of the magnitude of IPSC decrease (–28% w/cocaine versus –24% w/PD 128907), as well as the sensitivity to the selective D3 receptor antagonist U 99194, the actions of cocaine on the monosynaptic IPSC evoked following stimulation in the stratum radiatum can be fully accounted for via actions at the D3 receptor.
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). Similarly, we found that application of D3 receptor agonist significantly increased the ratio of the paired population spike responses (Fig. 4, A and B). PPD of the population spike prior to drug application (0.76 ± 0.07, n = 4) was converted to paired-pulse facilitation in the presence of PD 128907 at 0.3 (1.14 ± 0.06, n = 4) and 3 (1.39 ± 0.07, n = 4) µM. Interestingly, in addition to the persistent effect of dopamine on PPD that was blocked by pretreatment with the dopamine receptor antagonist spiroperidol, Gribkoff and Ashe (1984a) also reported an acute suppression of the initial population spike amplitude that was reversible and not prevented by spiroperidol. We did not observe any significant decrease in the amplitude of PS1 in the presence of PD 128907 (Fig. 4A). These findings suggests that one of these two previously reported actions of dopamine on the CA1 population spike can be attributed to the activation of D3 receptors (i.e., the persistent disinhibition), whereas the acute decrease of excitatory transmission is likely to be mediated by a different dopamine receptor subtype (Hsu, 1996; Otmakhova and Lisman, 1998).
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Cocaine Enhances Synaptic Excitation of Pyramidal Cells. If cocaine acts via D3 receptor activation and causes disinhibition, then it should enhance synaptic excitation of pyramidal neurons. To investigate this possibility, mixed EPSC-IPSC responses were evoked by stimulating in the stratum radiatum (Fig. 5C) in the absence of either glutamatergic or GABA-ergic antagonists. Following the application of cocaine (10 µM), the EPSC component was significantly enhanced (+30 ± 10%, p < 0.02), whereas the IPSC component of the mixed response was concomitantly decreased (-24 ± 10%) in these same cells (n = 6). Notably, the magnitude of the decrease in the IPSC component of the mixed EPSC-IPSC response observed under these conditions compares quite favorably with the decrease observed in the monosynaptic IPSC following either cocaine (–28%, Fig. 1B) or PD 128907 (–24%, Fig. 3A) application, suggesting that the modulation of ionotropic glutamatergic drive of GABA-ergic neurons is not a significant contributing factor to D3 receptor-mediated actions in this circuit. Additional evidence consistent with this inference is that cocaine does not significantly affect pharmacologically isolated EPSCs (+13 ± 12%, n = 7). Thus, both the population spike measure (Fig. 4A) and the intracellular measures (Figs. 1B and 5) are consistent with the conclusion that D3 receptor activation directly affects inhibitory circuitry in the CA1 and, as a result, indirectly modulates excitatory synaptic transmission.
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Our initial studies were motivated by our recently reported findings that acutely applied cocaine can act through dopamine transporter blockade to enhance neurotransmitter activation of D2-like dopaminergic receptors and significantly enhance the magnitude of LTP evoked in the CA1 region of hippocampal slices (Thompson et al., 2005). We also noted that Gribkoff and Ashe (1984a, using paired stimuli while recording population spike responses) had previously concluded that exogenously applied dopamine could elicit a long-lasting attenuation of inhibition in the CA1. As outlined in the previous paragraph, we have found strong support for such a disinhibitory mechanism of cocaine actions using whole-cell voltage-clamp recordings of monosynaptic IPSCs evoked following stimulation of the stratum radiatum in the CA1 region. Activation of the D3 subtype of dopamine receptor appeared to mediate this effect because a D3-selective agonist could mimic the actions of cocaine, and pretreatment with a selective D3 antagonist prevented significant effects of either cocaine or PD 128907.
The potential relevance of the endogenous dopamine transmitter system to hippocampal function is increasingly being recognized and incorporated into models for novelty detection and long-term memory (Lisman and Grace, 2005), and a significant amount of anatomical evidence has accumulated in support of an endogenous dopaminergic projection from mesencephalic structures such as the ventral tegmental area and the substantia nigra to the hippocampal formation (for review, see Gasbarri et al., 1997). Despite this, it remains the case that the absolute level of dopamine present in hippocampal tissue is quite low relative to the other monoamine transmitters. For example, one report of the levels of DA, norepinephrine, and 5-hydroxytryptamine in the CA1 region of ventral hippocampus indicates approximately 20-fold less DA than norepinephrine or 5-hydroxytryptamine (Hortnagl et al., 1991). Therefore, it is potentially significant that the dopamine receptor type we have identified as being likely to mediate the actions of cocaine on the IPSC is the D3 receptor because it has the highest affinity for dopamine among all of the five members of the DA receptor family (at a Ki of 25 nM, it has approximately 20-fold higher affinity than for the D2 receptor type; Sokoloff et al., 1990). This would potentially allow for significant activation of D3 receptors by endogenous dopamine during enhanced release or inhibited reuptake, despite the aforementioned relatively low absolute amount of DA known to be present in the tissue.
We propose that the D3 type of receptor is the most likely to mediate the observed effects of cocaine for the following reasons. First, the highly selective D1/5 antagonist SCH 23390 was ineffective when used at a concentration at least 1000-fold higher than its Ki for these sites. Second, the most selective antagonist tested for the D2-like family was U 99194, which has a 14-fold higher affinity for D3 sites compared with D2 sites, and the concentration used was approximately 6 times greater than its affinity for D3 sites and 13 times lower than its affinity for D2 sites. In addition, U 99194 exhibits a >60-fold preference for the D3 site as compared with D4 binding site (Audinot et al., 1998). Third, the D3-selective agonist PD 128907 was fully capable of mimicking the actions of cocaine, and this compound has been reported to have >300-fold preference for the D3 site as compared with D2 binding site (Audinot et al., 1998). The effectiveness of three different dopamine receptor antagonists to block cocaine's effects, along with the ability of a selective dopamine receptor agonist to mimic cocaine's effect on the IPSC, strongly suggests that the common property of these four distinct compounds is their actions at the D3 type of dopamine receptor and is not consistent with effects at a non specific (i.e., a nondopaminergic) site. Finally, Hsu (1996) reported that the evoked EPSP in CA1 was inhibited via activation of a D2 type of dopamine receptor, an effect that we also did not observe when PD 128907 was applied to the population response (Fig. 4) or when cocaine was applied to the evoked EPSC (Fig. 5). This suggests that neither cocaine nor PD 128907 was acting via D2 receptor activation under the conditions we have described.
Assuming activation of the D3 type of dopamine receptor is occurring following either cocaine or PD 128907 application, the mechanisms underlying the subsequent inhibition of the evoked IPSC is a topic of considerable interest. This dopamine receptor type has been localized in the CA1 to the neuropil of the stratum radiatum and stratum oriens (but not stratum lacunosum-moleculare; Khan et al., 1998), where several classes of GABA-ergic interneurons are located and where some tyrosine hydroxylase-like immunoreactivity has been reported (Milner and Bacon, 1989). This distribution contrasts with that of the D4 dopamine receptor type, which is most densely associated with the CA1 pyramidal cell body layer and also was found in all the strata containing the pyramidal cell dendritic processes (stratum oriens, stratum radiatum, and stratum lacunosum-moleculare). In comparison, the density of D2 immunostaining is relatively sparse in the CA1 (Khan, et al., 1998). The activation of D3 dopamine receptors has been shown to interact with multiple signal transduction pathways, including acting to inhibit adenylate cyclase, inhibit calcium currents, and enhance potassium currents (for review, see Missale et al., 1998). Assuming that D3 receptors are associated with nonpyramidal neurons in the CA1 region of the hippocampus, any of these generally inhibitory consequences could underlie the disinhibition we have described at the level of pyramidal cell activation. Our inability to reverse the cocaine-induced decrease in the IPSC with antagonist is consistent with prior observations describing the long-lived nature of some of the effects of dopamine in the CA1 (Gribkoff and Ashe, 1984a,b) and also indicates that the activation of a signaling cascade has occurred that persists beyond receptor occupancy by agonist. More definitive characterization of this signaling mechanism will require additional experiments that include recording from the D3 receptor-bearing cell and observing the direct effects of D3 receptor activation.
In conclusion, in this report, we have described a novel, specific role for the D3 subtype of dopamine receptor in modulating synaptic function in the CA1 region of the hippocampus. The D3 receptor-mediated inhibition of GABAergic influence in the CA1 could facilitate the limbic hyperactivity previously associated with schizophrenic symptoms (Krieckhaus et al., 1992; Heckers, 2001) and may also contribute to the persisting alterations in behavioral responses that occur following exposure to drugs of abuse (Caine and Koob, 1993; Vorel et al., 2002). D3 receptor-mediated disinhibition is likely to be a key mechanism by which dopamine can impact the processing of neuronal signals through hippocampal circuitry and thereby potentially contribute to the maladaptive states associated with drug addiction and schizophrenia.
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Acknowledgements |
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Footnotes |
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ABBREVIATIONS: LTP, long-term potentiation; IPSC, inhibitory postsynaptic current; ACSF, artificial cerebrospinal fluid; EPSC, excitatory postsynaptic current; QX314, N-(2,6-dimethylphenylcarbamoylmethyl)triethylammonium bromide; PS, population spike; PD 128907, (+)-(4aR, 10bR)-3,4,4a,10b-tetrahydro-4-propyl-2H,5H-[1]-benzopyrano-[4,3-b]-1,4-oxazin-9-ol; U 99194, 5,6-dimethoxy-indan-2-yl dipropylamine; SCH 23390, R-(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine; PPD, paired-pulse depression; DA, dopamine.
Address correspondence to: Dr. John J. Wagner, Department of Physiology and Pharmacology, 501 D.W. Brooks Drive, Athens, GA 30602-7389. E-mail: jwagner{at}vet.uga.edu
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