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Application of 
-methyl-
d
-aspartate induces long-term potentiationin the medial perforant path and long-term depression in the lateralperforant path of the rat dentate gyrus in vitro
Anthony M. Rush
a
, Michael J. Rowan
b
, Roger Anwyl
a,
*
Department of Physiology, Trinity College, Dublin 2, Ireland 
Department of Pharmacology and Therapeutics; Trinity College; Dublin 2, Ireland 
Received 22 August 2000; received in revised form 30 November 2000; accepted 30 November 2000
Abstract
The effect of application of 
-methyl-
d
-aspartate (NMDA) on synaptic plasticity was studied in the medial and lateralperforant path-granule cell synapse in the outer blade of the dentate gyrus in vitro. Field excitatory post-synapticpotentials were recorded from the middle or outer molecular layer in response to stimulation of the medial or lateralperforant path. Bath perfusion of NMDA (10
m
M, 5 min) resulted in induction of long-term potentiation in the medialperforant path, and induction of long-term depression in the lateral perforant path.
q
2001 Elsevier Science Ireland Ltd.All rights reserved.
Keywords 
: Long-term potentiation; Long-term depression; Dentate gyrus;
-Methyl-
d
-aspartate
It is now well established that long-lasting changes inglutamatergic synaptic transmission can be induced byappropriate stimulation in many areas of the mammalianbrain [3]. Two forms of synaptic plasticity have been parti-cularly frequently studied, long-term potentiation (LTP) [4]and long-term depression (LTD) [7,16], which are inducedby brief high frequency stimulation (HFS) and prolongedlow frequency stimulation (LFS), respectively. Both LTPand LTD have forms that are dependent upon activationof 
-methyl-
d
-aspartate (NMDA) receptors, and accord-ingly they are inhibited by the NMDA receptor antagonist
d
-2-amino-5-phosphonopentanoate (
d
-AP5) [6,7,16]. Brief application of NMDA in control physiological media hasbeen shown in several previous studies in CA1 to induceeither a transient depression of the test ®eld excitatory post-synaptic potential (EPSP) followed by a short-lasting poten-tiation [6,9,14,15], or recently, LTD [10]. However, NMDAhas not been shown to induce LTP when applied in controlphysiological media. In the present studies, the effect of NMDA application has been investigated in the medialand lateral perforant paths of the dentate gyrus in vitro.We show that NMDA perfusion has a differing effect onplasticity in the medial and lateral perforant paths, inducingLTP in the former and LTD in the latter.Allexperimentswerecarriedoutontransverseslicesoftherat hippocampus (age 3±4 weeks, weight 40±80 g). Thebrains were rapidly removed after decapitation and placedincoldoxygenated(95%O
2
 /5%CO
2
)media.Sliceswerecutat a thickness of 350
m
m using a Campden vibroslice, andplacedinastoragecontainercontainingoxygenatedmediaatroom temperature (20±22
8
C). The slices were then trans-ferred as required to a recording chamber for submergedslices and continuously superfused at a rate of 5±7 ml/minat 30±32
8
C. The control media contained: (mM) NaCl 120;KCl2.5;NaH
2
PO
4
1.25;NaHCO
3
26;MgSO
4
2.0;CaCl
2
2.0;
d
-glucose 10. All solutions contained 50
m
M picrotoxin(Sigma) to block 
g
-aminobutyric acid
A
-mediated activity.EPSPswererecordedinthemedialandlateralperforantpath-way intheouterbladeofthedentate gyrus. Standardelectro-physiologicaltechniqueswereusedtorecord®eldpotentials.Presynaptic stimulation was applied to the medial or lateralperforantpathwayofthedentategyrus,and®eldEPSPswererecorded at a control test frequency of 0.033 or 0.0166 Hzfrom the middle or outer one-third of the molecular layer of thedentategyrus.Tocheckpathwayspeci®city,paired-pulsestimuliweregiven(40msapart)andpaired-pulsedepressionorfacilitationusedascriteriatocon®rmcorrectplacementinthe medial or lateral perforant pathways, respectively. In
Neuroscience Letters 298 (2001) 175±1780304-3940/01/$ - see front matter
q
2001 Elsevier Science Ireland Ltd. All rights reserved.PII: S0304-3940(00)01742-0www.elsevier.com/locate/neulet* Corresponding author. Tel.:
1
353-1-6081-624; fax:
1
353-1-679-3545.
E-mail address: 
ranwyl@tcd.ie (R. Anwyl).
 
A.M. Rush et al. / Neuroscience Letters 298 (2001) 175±178 
176
Fig. 1. NMDA induces LTP in the medial perforant path of the dentategyrus in vitro. (A) Bath perfusion of NMDA (10
m
M, 5 min) inducedaninitialsmallnon-signi®cantdepressionfollowed,uponwashoutoftheNMDA,asigni®cantLTPmeasuring21
^
5%,
6.(B)Repeatapplications of NMDA induced additional LTP which reached a maximum of 31
^
11%,
6. Subsequent HFS was still able to inducelarge additional LTP. (C) HFS-induced LTP following NMDA induced LTP of 58
^
7%,
6 (open circles) has a very similar amplitude tocontrol HFS-induced LTP of 50
^
6%,
7 (®lled circles). (D) Cessation of test stimulation during application of NMDA still resulted ininduction of LTP. (E) Paired pulse depression was not signi®cantly altered by induction of NMDA-mediated LTP.
 
each experiment, an input-output curve (afferent stimulusintensity versus EPSP amplitude) was plotted at the testfrequency. For all experiments, the amplitude of the testEPSP was adjusted to one-third of maximum, usually about1±1.2 mV. LTP/LTD was measured at 25±30 min postNMDA application. HFS-induced LTP was induced byeighttrainseachofeightstimuliat200Hz,intertraininterval0.2 s. NMDA was obtained from Sigma. Recordings wereanalyzed using p-Clamp. Values are the mean
^
SEM for
n
slices and two-tailed Student's
-test was used for statisticalcomparison.In previous experiments in CA1, perfusion of a relativelyhigh concentration (150
m
M) of NMDA for a brief timeinduced a large transient depression followed by a transientpotentiation [14,15]. Similar ®ndings were observed in thepresent study in the dentate gyrus using a high concentrationofNMDAforabrieftime.More recent workinCA1showedthat longer bath application of NMDA (20
m
M for 3 min)inducedaSTD,followedbyaLTD[10].Wethereforeinves-tigated the effect of a lower concentration of NMDA (10±20
m
M)perfusedforalongerperiod(5min)inthedentate.Intheinitial set of experiments, recordings were made from themedial perforant path. Bath perfusion of NMDA (10
m
M, 5min)causedasmall(1±5%)butnon-signi®cantdepressionof the EPSP during the actual perfusion, followed, upon wash-out, by an increasing enhancement of the EPSP over thesubsequent 10 min and then induction of a stable LTPmeasuring 21
^
5% (
n
6) (Fig. 1A). Repeat applicationsofNMDAinducedadditionalLTP,withtheNMDA-inducedLTPreachingamaximumof31
^
11%;
n
6afterthethirdapplication of NMDA (Fig. 1B). Such NMDA-induced LTPdid not occlude HFS induced LTP. Thus control HFS-inducedLTPmeasured50
^
6%;
n
7(Fig.1C).Followingmaximal induction of LTP by NMDA application, themagnitude of HFS-induced LTP was not altered, measuring58
^
7%;
n
6(Fig. 1B,C).Stimulationduring theapplica-tion of NMDA was not found to be necessary for the induc-tion of LTP. Thus cessation of test stimulation during and 15min after the perfusion of NMDA did not inhibit the induc-tion of LTP, which measured 19
^
3;
n
5 (Fig. 1D). In themedial perforant path, paired stimuli applied at 40 ms inter-pulse interval results in paired pulse depression of the EPSPof16
^
3%;
n
6.ThepairedpulsedepressionwasreducedinthepresenceofNMDA,to5
^
4%,butfollowingwashoutof NMDA, returned to the control level, i.e. no change inpaired pulse depression accompanied NMDA induced LTP(Fig. 1E).Recordings from the lateral perforant path showed thatapplication of NMDA had a very different action to that inthe medial perforant path. Thus perfusion of NMDA (10
m
M, 5 min) induced LTD of the test EPSP. The LTDinduced by a single application of NMDA was small andnot signi®cant. However, additional applications of NMDAproduced a summation of the LTD, and LTD became promi-nent, measuring 25
^
5%;
n
4, after the 2nd to 4th appli-cation (Fig. 2).The present study demonstrates that the plasticity evokedby NMDA has a regional speci®city. In the medial perforantpath of the dentate gyrus, NMDA induces LTP, whereas inthe lateral perforant path, NMDA induces LTD. The ®ndingthatNMDAapplicationcaninduceLTPinthemedialperfor-antpathisthe®rstsuchobservationofNMDA-inducedLTP.PreviousstudieshaveshownthatNMDAapplicationinduceseither only a short-term potentiation when relatively highconcentrations ofNMDAwereappliedforabrieftimeeither[6,9,14,15]orLTDwhenlowconcentrationsofNMDAwereapplied for a longer time [10]. The induction of LTP byNMDA in the medial perforant path in the present study,rather than short-term potentiation, is likely to be due to theapplication of NMDA at a low concentration and for a rela-tively prolonged period. Interestingly, the LTP induced byexogenous NMDA application did not occlude with HFS-inducedLTP.ThiscouldbeduetodifferentsitesofinductionoftheLTPinducedbyexogenousNMDAapplication andbyHFS. For example, perhaps exogenous NMDA applicationresults in a presynaptic site for LTP induction via activationof presynaptic NMDAR [5] or NMDA receptors located onastrocytes, as suggested by Araque et al. [1], in contrast toHFS inducing LTP at a post-synaptic site. As no measurablechanges in paired-pulse depression accompanied the LTPinduced by exogenous NMDA application, such LTP, if presynaptic, would involve a change in the number of sitesof release rather than a change in release probability. Thedetailed mechanisms of induction of the LTP induced byexogenous NMDA are presently under investigation. TheinductionofLTDbyNMDAapplicationinthelateralperfor-ant path is identical to that found in the study [10] in CA1, inwhich a similar concentration and duration of application of NMDA to the present study was used.It is well established that Ca
2
1
in¯ux via NMDA receptor
A.M. Rush et al. / Neuroscience Letters 298 (2001) 175±178 
177
Fig. 2. NMDA induces LTD in the lateral perforant path of thedentate gyrus in vitro. An initial application of NMDA by bathperfusion did not induce LTD, but further applications inducedsigni®cantLTD measuring25
^
5,
4, after the 4th applicationof NMDA.
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