Behavioural Brain Research 159 (2005) 105–111

Research report

Noradrenaline involvement in the memory-enhancing effects ofexposure to a complex rhythm stimulus following discriminated

passive avoidance training in the young chick

S.R. Toukhsatia,∗, N.S. Rickarda, E. Perinia, K.T. Nga, M.E. Gibbsb

a Psychology Department, Monash University, Caulfield East 3145, Vic., Australiab Department of Pharmacology, Monash University, Clayton 3800, Vic., Australia

Received 4 June 2004; received in revised form 11 October 2004; accepted 16 October 2004Available online 23 November 2004

Abstract

Previous research in our laboratory has demonstrated a significant memory-enhancing effect of exposure to a complex rhythm stimulusfollowing weakly-reinforced passive avoidance learning in chicks. The aim of this study was to explore whether noradrenaline mediates thisp red beads.I ousal levelsw l showedt ist,p uggest thatt ysiologicala©

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rocess. Chicks were trained on a strongly-reinforced single-trial passive avoidance task involving discrimination between two colountracerebral administration of the protein synthesis blocker, anisomycin, revealed that a phase of memory formation sensitive to aras extended by approximately 35 min following exposure to the complex rhythm stimulus. Administration of 2,4-dinitropheno

hat this extension occurred during phase B of intermediate-term memory. Finally, a higher dose of the�-adrenergic receptor antagonropranolol, was required to inhibit long-term memory in the presence of the auditory stimulus than in its absence. These findings s

he memory-enhancing effects of the complex rhythm stimulus may be mediated by noradrenaline, possibly via an increase in phrousal.2004 Elsevier B.V. All rights reserved.

eywords:Passive avoidance learning; Day-old chick; Auditory rhythm; Arousal; Long-term memory consolidation; Anisomycin; 2,4-Dinitrophenololol

. Introduction

There is some evidence that exposure to rhythmic audi-ory stimuli may increase physiological arousal[9,24,29]asell as enhance learning (see[23]). Moreover, an increase

n physiological arousal has been proposed to account forhe facilitation of various aspects of cognition by auditorytimuli [8,28,36]. It can be speculated, therefore, that pre-ious findings in our laboratory showing a strong memory-nhancing effect of exposure to a complex rhythm stimulusCRS) following weakly-reinforced passive avoidance train-ng (see[38,39]), may be attributable to changes in arousal,

∗ Corresponding author. Tel.: +61 3 9903 2367; fax: +61 3 9903 2501.E-mail address:samia.toukhsati@med.monash.edu.au

S.R. Toukhsati).

which in this context is taken to encapsulate changes irelease of stress-related hormones. This proposition is cotent with research that has shown long-term memory (Lconsolidation in weakly-reinforced chicks, following theministration of arousal- or stress-related hormones, sucorticosterone[14,35]and noradrenaline[5].

The Gibbs and Ng[13], three-stage memory model pvides an ideal paradigm with which to determine whethememory-enhancing effects of exposure to the CRS arediated by arousal- or stress-related hormones. One horof particular interest in the current context is noradrena(NA), which has been shown to be involved in the formaof relatively permanent memory[4]. According to this modethe memory trace is delineated by retention deficits 1555 min post-training and is comprised of short-term mory, labile or intermediate-term memory (ITM) (divided in

166-4328/$ – see front matter © 2004 Elsevier B.V. All rights reserved.oi:10.1016/j.bbr.2004.10.007

106 S.R. Toukhsati et al. / Behavioural Brain Research 159 (2005) 105–111

phases A and B), and LTM. These stages are thought to be se-quentially linked such that consolidation of the learning taskinto LTM is dependent upon the appearance of ITM phaseB (ITMB), which extends from 30 to 55 min after strongly-reinforced training[32].

The initiation of ITMB appears to be dependent upon thestate of arousal around the time of training, which is deter-mined, at least in part, by the strength of the training stimulus[2,11]. However, changes in levels of NA alter the temporalparameters of the memory trace, irrespective of the strengthof reinforcement[16]. That is, the duration of ITM is mod-erated by stress (such as isolation) and/or administration ofhormones[2,7,16,20,34]. For example, Gibbs and colleagues[4,14,31]found that subcutaneous administration of corticos-terone (CS), adrenocorticotropic hormone (ACTH) or nora-drenaline immediately after strongly-reinforced training, de-layed the onset of LTM for the passive avoidance task by25 min, such that the second retention deficit occurred at80 min post-training.

The aim of the experiments reported here was to estab-lish whether exposure to a CRS produces effects similar tothose observed when memory is modulated by hormonesthat are associated with arousal or stress such as NA. Theinvolvement of such hormones can be inferred by an ex-tended duration of ITM in chicks trained using a strongly-reinforced version of the single-trial passive avoidance task.P theC ethy-l to rcedt foro inis-tt cedt , wasu

2

2

orpc n them earchP

2

tor[ mMc g-i isma ntra-t ra l/hem[ har-

macological control. All drugs were obtained from Sigma ChemicalCompany, St. Louis, USA.

Drugs were dissolved in physiological saline solution, and 10�lvolume injected freehand into the forebrain of each hemisphere us-ing a Hamilton repeat-dispensing syringe (500�l capacity). A 27-gauge needle was attached to the syringe, and a plastic sleeve en-sured that the needle was injected to a regulated depth of 3–3.5 mm,enabling accurate administration into the targeted region[20]. Theinjection site was the hyperstriatal region of the forebrain, a re-gion known to be implicated in memory processing for this task[21,27,33].

2.3. Apparatus and procedure

A detailed description of the apparatus and procedures used inthis study has been provided in a previous publication (see[38]).Briefly, young chicks were pre-trained to peck at water-coated redand blue glass beads (4 mm diameter) for 10 s each. After resting for30 min, chicks were trained on a strongly-reinforced version of thesingle-trial passive avoidance task, for which they were presentedfor 10 s with a red glass bead coated in 100% MeA (APS AjaxFinechem, Auburn, Australia). Chicks that did not peck the train-ing bead within 10 s of bead presentation, as indicated by latencydata, were excluded from further analysis at the conclusion of datacollection.

Retention for the task was tested 100 min post-training (unlessotherwise stated) by presenting chicks with a dry red and dry blueglass bead each for 10 s. Chicks failing to peck the blue bead dur-i weree ent.R ratio( d byt sting.A es ani

enti-cc ing( e pa-r k fol-l eda e lev-ec aticn withl it-tp uresw prac-t sixthe

3f

isd ning,w st-t until

reviously, memory enhancement following exposure toRS has been demonstrated using a weak dilution of m

anthranilate (MeA) (see[38,39]). However, ITMB is nobserved in chicks that have been given weakly-reinfo

raining [3,4,11]. Rather, memory tends to be presentnly a short period after training, unless chicks are adm

ered hormones, such as NA and ACTH[4]. To explore theemporal parameters of ITM, therefore, strongly-reinforraining, which generates a permanent memory tracesed.

. General method

.1. Subjects

One to two-day-old White Leghorn cross Black-Australockerels were used in all experiments and were obtained oorning of each experimental day from a local hatchery (Resoultry Farm, Vic., Australia).

.2. Drugs

Anisomycin (ANI), a well-known protein-synthesis inhibi12], was bilaterally injected at a dose of 38 nmol/hem (3.8oncentration)[13] immediately after training. The pharmacolo

cal agent, 2,4-dinitrophenol (DNP) inhibits oxidative metabolnd was administered at a dose of 2 nmol/hem (0.2 mM conce

ion) [15]. Propranolol, a selective�1- and�2-adrenergic receptontagonist, was injected bilaterally at a dose of 3, 10 or 30 nmo

18]. Finally, physiological saline (154 mM) was used as the p

ng the test trial, and demonstrating generalised avoidance,xcluded from further analysis at the conclusion of the experimetention levels were indexed using a mean discrimination

MDR), defined as the number of pecks to the blue bead dividehe summation of pecks to the red and blue beads during tevoidance of the red bead and pecking of the blue bead provid

ndex of discrimination memory for the task.The notation and a schematic of the CRS, which was id

al to that used and described in detail, previously (see[38,39])an be seen inFig. 1. The CRS was presented 5 min post-trainunless otherwise stated), and for duration of 1 min, which arameters that have been found to promote retention of this tasowing weakly-reinforced training[38]. The stimulus was presentt a sound pressure level of 10 dB(A) above background noisls in accordance with recent research findings[39]. The auditoryontrol condition was background laboratory noise (no systemoise, NSN) which comprised mainly of silence interspersed

ow frequency humming from an air conditioner and chick ‘twers’, the presence of which is associated with alertness[1]. Theharmacological control was physiological saline. All procedere conducted in accordance with the Australian code of

ice for the care and use of animals for scientific purposes (dition 1997).

. Experiment 1: extension of intermediate memoryollowing exposure to the complex rhythm stimulus

In the Gibbs and Ng[13] model, the protein synthesependent LTM stage is expressed by 60 min post-traiith ANI inducing retention loss beginning at 55 min po

raining. It is argued, therefore, that the ITM stage lasts

S.R. Toukhsati et al. / Behavioural Brain Research 159 (2005) 105–111 107

Fig. 1. The complex rhythm stimulus: (a) notation and (b) schematic (grey shading denotes an accented pulse).

50 min post-training, with the transition to the LTM stageoccurring at around 55 min. As mentioned previously, hor-mones such as NA, ACTH and CS extend the duration ofITM until around 80–90 min following training[15]. If theCRS promotes retention through the release of arousal hor-mones, it should extend the duration of ITM beyond 50 min,in the same way that exogenous administration of these hor-mones has been shown to do. It would follow, therefore, thatin the presence of the CRS, protein synthesis inhibitors suchas ANI should result in loss of memory occurring some timelater than 55 min post-training. The aim in this experimentwas to test this hypothesis.

3.1. Method

Chicks (N= 130) were trained on the strongly-reinforcedversion of the passive avoidance task described in the Sec-tion 2. With the exception of the auditory control NSN con-dition, different groups of 20 chicks were exposed to theCRS for duration of 1 min, presented 5 min post-training,at an intensity of 10 dB(A) above background noise lev-els. Chicks were administered 38 nmol/hem ANI immedi-ately after strongly-reinforced training. Different groups of20 treatment chicks were tested at 60, 70, 80, 90, 100or 120 min post-training to establish the duration of ITM.Control (NSN-exposed) chicks were tested 70 min post-t

3

fters y fort minp A)i ,p tmentg cesi ost-t ing( TM

Fig. 2. The effects of strongly-reinforced training (100% MeA), immedi-ately followed by bilateral injections of anisomycin (0 min post-training).Error bars indicate the standard error of the mean. With the exception ofthe control group (NSN, no systematic noise), all chicks were exposed to1 min of the complex rhythm stimulus (CRS), presented 5 min post-training,at 10 dB(A) above background noise levels, and were tested at various timespost-training. The NSN control group was tested at 70 min post-training,* p< 0.05.

was extended some 35 min following exposure to the CRSbeyond the usual 55 min endpoint.

4. Experiment 2: extension of phase B of theintermediate memory stage following exposure to thecomplex rhythm stimulus

The two phases of ITM can be differentiated on the basisthat the formation and maintenance of ITMA can be dis-rupted by intracranial injections of the inhibitor of oxida-tive phosphorylation, DNP[2,16,30]. The maintenance ofITMA is dependent upon oxidative metabolism and is im-paired within 10 min of DNP administration, given between5 and 25 min post-training, but not after 25 min[15,32]. Ifthe duration of ITMA is extended, however, the time win-dow during which DNP can be administered and still blockmemory is also lengthened. Therefore, the phase of ITM,which has been extended by CRS exposure can be revealedby the time window during which DNP produces amnesia[2].

raining.

.2. Results and discussion

Fig. 2 shows that chicks exposed to the CRS atrongly-reinforced training demonstrated good memorhe single-trial passive avoidance task until at least 90ost-training. A one-way analysis of variance (ANOV

ndicated a significant treatment effect,F(6, 123) = 8.13< 0.001. Post hoc Dunnett’s tests comparing each trearoup to the control condition revealed significant differen

n MDRs for chicks tested at 60, 70, 80, and 90 min praining (p< 0.01) but not at 100 or 120 min post-trainp< 0.05). These findings indicate that the duration of I

108 S.R. Toukhsati et al. / Behavioural Brain Research 159 (2005) 105–111

The aim in this experiment was to examine whether theextension of ITM following exposure to the CRS was duringITMA, ITMB or both. Previously, it was shown that expo-sure to the CRS extended the duration of ITM by at least30 min. If this extension is during ITMA, then DNP shouldblock retention when administered at any time between 10and 55 min post-training; that is, 30 min longer than the du-ration for which it is usually inhibitory. In contrast, if ITMBis extended by exposure to the CRS, then DNP should onlybe an effective amnestic agent when administered between10 and 25 min post-training, since ITMA remains the sameduration and susceptible to metabolic inhibition as in controlchicks.

4.1. Method

Chicks (N= 301) were trained on the strongly-reinforcedversion of the passive avoidance task described in the Section2. Chicks were administered a dose of 2 nmol/hem (0.2 mMconcentration) DNP 10, 30, 35, 40, 45 or 50 min follow-ing strongly-reinforced training. Treatment chicks were ex-posed to the CRS for duration of 1 min, presented 5 minpost-training, at an intensity of 10 dB(A) above backgroundnoise. Control chicks were exposed to the NSN condition.All chicks were tested for retention of the passive avoidancetask at 100 min post-training.

4

cesi icksi -c ,b find-i be-y cks( thee ringI

F ereda day-o s weree r thea nted5 icksw

5. Experiment 3: noradrenaline involvement in theextension of intermediate memory, phase B, followingexposure to the complex rhythm stimulus

The permanence of a memory trace is largely determinedby the state of arousal around the time of learning[5,10,22].Experiments 1 and 2 have shown that exposure to the CRSis likely to promote memory by increasing arousal levelsin the chick. However, these data do not differentiate be-tween the various arousal/stress hormones. There is goodreason to believe that NA is the most likely candidate forthis role. NA is released in the brain and has been shown tobe essential for the consolidation of LTM[5,17,20,25,26].Central injection of NA into the intermediate medial hy-perstriatum ventrale (IMHV) activates different adrenocep-tor subtypes, depending on the dose of noradrenaline[21].For instance, a moderate dose of NA, which may be as-sociated with attention, activates�3-adrenoceptors. As thedose of NA increases,�2-adrenoceptors are activated andduring stress,�1-adrenoceptors are activated[20]. In theircomprehensive review, Gibbs and Summers[20] noted twocritical periods for NA involvement in memory consolida-tion: (a) during acquisition and (b) during consolidation,when the labile memory trace is transformed into its per-manent form. Provided the level of the reinforcement issufficient, there is evidence to suggest that NA is releaseds sei task[

pas-s con-d his� redi in,5 hem[ So then ah d toi ouldb udi-t slyb cep-t dS oft -a n-j se ofm ntlyh ns ofp

them utedt igherd iredt SNc

.2. Results and discussion

Fig. 3 shows that there were no significant differenn retention levels of CRS-treated and NSN-treated chnjected with DNP. A two-way ANOVA indicated signifiant time of administration effect,F(1, 214) = 6.20,p< 0.001ut no significant treatment or interaction effect. These

ngs reveal that ITM phase A (ITMA) was not extendedond the duration typically evident in strongly-trained chi30 min post-training). Accordingly, this study shows thatxtension of ITM demonstrated in Experiment 1 is duTMB.

ig. 3. The effects of bilateral injections of 2,4-dinitrophenol administt various times relative to strongly-reinforced training (100% MeA) told chicks. Error bars represent standard errors of the mean. Chickxposed to either the auditory control (NSN, no systematic noise), ouditory treatment (CRS, complex rhythm stimulus) for 1 min, presemin post-training, at 10 dB(A) above background noise levels. All chere tested for retention 100 min post-training.

hortly before ITMB to initiate the formation of this phan the chick trained on a discriminative avoidance5,20].

Previous studies have shown that memory for theive avoidance task, under normal strongly-reinforceditions, is impaired by the NA blocker, propranolol. T-adrenergic blocker inhibits retention when administe

ntracranially into the IMHV region of the chick forebra–25 min post-training, at a dose of either 10 or 30 nmol/

20]. If the extension of ITM following exposure to the CRbserved earlier was due to an increased release of NA,igher dose of propranolol should theoretically be require

nhibit memory in the presence of the CRS (since there we higher levels of endogenous NA available) than in a

ory control NSN chicks. This methodology has previoueen used effectively to demonstrate the role of adreno

ors in memory for this task[18,19]. For example, Gibbs anummers[19] challenged the memory inhibiting effects

he intracerebrally administered�1—AR agonist, methoxmine with the selective�1—AR antagonist, prazosin (i

ected subcutaneously). It was determined that the doethoxamine required to inhibit memory was significaigher when chicks also received subcutaneous injectiorazosin.

The aim of this experiment was to explore whetheremory-enhancing effects of the CRS could be attrib

o an increased release of NA by assessing whether hoses of the�-adrenergic blocker, propranolol, were requ

o inhibit memory in the presence of the CRS than in Nontrol chicks.

S.R. Toukhsati et al. / Behavioural Brain Research 159 (2005) 105–111 109

5.1. Method

Chicks (N= 148) were trained on a strongly-reinforcedversion of the single-trial passive avoidance task. On eachexperimental day, two groups of chicks were exposed to theCRS for duration of 1 min, presented 10 min post-training,at an intensity of 10 dB(A) above background noise levels;another two groups of chicks were not exposed to any au-ditory treatment condition (NSN control). All chicks werebilaterally injected intracranially into the IMHV with pro-pranolol, 5 min post-training, at a dose of 0 (saline), 3, 10, or30 nmol/hem. Saline and 3 nmol/hem propranolol have beenshown to have no effect on retention[20] and thus acted asnegative controls for both NSN and CRS chicks. All chickswere tested for retention 100 min post-training.

5.2. Results and discussion

Fig. 4 reveals the effect of exposure to the NSN controlcondition or the CRS, preceded by injections of propranololor saline, on LTM for the strongly-reinforced passive avoid-ance task. A two-way ANOVA revealed a significant maineffect of auditory stimulus,F(1, 140) = 5.09,p< 0.05, a sig-nificant main effect of drug,F(3, 140) = 20.82,p< 0.001, anda significant interaction,F(3, 140) = 5.59,p< 0.001. Post hocs ncesi ad-mT cksa RS,t on-s

ve fort tot t is,a o-n RS-

F ex-p con-s afters ctedw osedt minp ing,*

treated chicks (30 nmol/hem) than was necessary in strongly-reinforced NSN control group chicks (10 nmol/hem). Thenon-inhibitory effects of 10 nmol/hem injections of propra-nolol, following exposure to the CRS, suggest that exposureto this auditory stimulus may increase the release of NA; thememory-enhancing effects of which are blocked by a dose of30 nmol/hem propranolol.

6. General discussion

The findings presented in this study suggest that thememory-enhancing effects of exposure to the CRS may bemediated by NA. Support for this proposition is three-fold.First, it was shown that the duration of ITM, following expo-sure to the CRS, was extended to at least 90 min post-training.Past research (see[16]) has shown that an extension of ITMtypically occurs with administration of exogenous hormones.

Second, the effective times of administration of themetabolic inhibitor DNP were the same for treatment (CRS)and control (NSN) chicks, suggesting that the duration ofITMA was similar in both groups. Accordingly, the exten-sion of ITM must have been during phase B, the expressionof which is known to be modulated by NA[2,16,20].

Third, it was established that a considerably higher doseof the�-adrenergic receptor antagonist, propranolol, was re-q ed tot d toN ma-n ly-t doseo ings[ in-h inC ausesa ma-te cantcT NAr ef-f , dataf istentw tionf

h re tot hiten mon-s RSw erel theC lancet ks,s re-l -

imple main effects analyses revealed significant differen retention levels of CRS and NSN chicks only when

inistered propranolol at a dose of 10 nmol/hem (p< 0.001).here was no significant difference in the number of pet the blue test bead for chicks exposed to NSN and C

(38) = 0.91,p< 0.05, suggesting that the CRS had no npecific effect on the response to the blue bead.

These results suggest that the dose-response curhe inhibiting effect of propranolol on recall was shiftedhe right in chicks that were exposed to the CRS. Tha

considerably higher dose of the�-adrenoceptor antagist, propranolol, was required to block retention in C

ig. 4. The effects of intracerebral injections of propranolol, prior toosure to the CRS (complex rhythm stimulus), on long-term memoryolidation. Error bars indicate standard errors of the mean. At 5 mintrongly-reinforced training, groups of 20 chicks were bilaterally injeith various doses of propranolol or saline, after which they were exp

o the CRS (+10 dB(A)) or NSN (no systematic noise) control at 10ost-training. All chicks were tested for retention at 100 min post-trainp< 0.05.

uired to impair retention in chicks that had been exposhe CRS (30 nmol/hem), in comparison to chicks exposeSN (10 nmol/hem). The finding that the formation of perent memory was inhibited in NSN control chicks strong

rained on the passive avoidance task and injected with af 10 nmol/hem propranolol replicates past research find

20]. Most importantly, the finding that retention wasibited by 30 nmol/hem propranolol, but not 10nmol/hemRS-treated chicks, suggests that exposure to the CRS cn increase in the release of NA. The role of NA in the for

ion of lasting memories is well documented[5,6,17,20]. Forxample, the appearance of ITMB coincides with signifihanges in levels of forebrain NA in the young chick[6].hese findings provide support for the hypothesis thatelease is likely to be involved in the memory-enhancingects of exposure to the CRS. Moreover, taken togetherrom each of the experiments presented here are consith the proposition that the effect of the CRS, on reten

or this task, is due to increased physiological arousal.It should be noted that previous findings (see[38,39])

ave illustrated a memory-enhancing effect of exposuhe CRS, but not to an isochronous rhythm stimulus, woise or human environmental noise. Such selectivity detrates that the facilitatory effects of exposure to the Cere not simply due to auditory stimulation, but instead w

ikely to be attributable to acoustic parameters specific toRS. Further, this stimulus bears some acoustic resemb

o ethologically relevant auditory stimuli for young chicuch as the maternal hen ‘food’ and ‘follow me’ calls. Piminary findings from our laboratory[37] suggest that expo

110 S.R. Toukhsati et al. / Behavioural Brain Research 159 (2005) 105–111

sure to these rhythmic calls also promotes LTM consolidationfor the weakly-reinforced passive avoidance task. Moreover,exposure to a synthesised 1 kHz maternal hen ‘food call’,in which the contextual information provided by frequencycharacteristics was reduced, enhanced LTM consolidation. Incontrast, exposure to the non-rhythmic maternal hen ‘roost-ing call’ does not appear to produce a memory-enhancing ef-fect. These findings support the proposition that rhythmicityis a prominent feature of memory-enhancing auditory stimuli[37].

The current findings implicate a role for NA, in additionto which, it is possible that exposure to the CRS also triggersan increase in the release of other hormones, such as CS,which may have been responsible for the extension of ITM.Nonetheless, observations made in past research, togetherwith the findings presented here, and are consistent with theproposition that the memory-enhancing effects of exposureto the CRS appear to be mediated by NA, possibly due tochanges in physiological arousal.

Acknowledgments

We would like to gratefully acknowledge the support re-ceived from the Monash University Postgraduate Publica-t Ed-w

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[12] Gibbs ME, Andrew RJ, Ng KT. Hemispheric lateralization of mem-ory stages for discriminated avoidance learning in the chick. BehavBrain Res 2003;139:157–65.

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[17] Gibbs ME, Summers RJ. Separate roles for�2- and�3-adrenoceptorsin memory consolidation. Neuroscience 2000;95:913–22.

[18] Gibbs ME, Summers RJ. Enhancement of memory consolida-tion in chicks by beta(3)-adrenoceptor agonists. Eur J Pharmacol2001;413:235–40.

[19] Gibbs ME, Summers RJ. Stimulation of�1-adrenoceptors inhibitsmemory consolidation in the chick. Eur J Neurosci 2001;14:1369–76.

[20] Gibbs ME, Summers RJ. Role of adrenoceptor subtypes in memoryconsolidation. Prog Neurobiol 2002;67:345–91.

[21] Gibbs ME, Summers RJ. Alpha 2-adrenoceptors in the basal gangliahave a role in memory consolidation and reinforcement. Neurophar-macology 2003;45:355–67.

[22] Gold PE, McGaugh JL. Hormones and memory. Adv Biochem Psy-chopharmacol 1977;17:127–43.

[23] Hetland L. Listening to music enhances spatial-temporal reasoning:48.

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[ ortex–89.

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ions Award and the laboratory assistance of Dr. Tomards.

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