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CNS & Neurological Disorders - Drug Targets

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ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

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One-Trial Appetitive Learning Tasks for Drug Targeting

Author(s): Robert Lalonde* and Catherine Strazielle

Volume 23, Issue 6, 2024

Published on: 15 June, 2023

Page: [680 - 686] Pages: 7

DOI: 10.2174/1871527322666230607152758

Price: $65

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Abstract

One-trial appetitive learning developed from one-trial passive avoidance learning as a standard test of retrograde amnesia. It consists of one learning trial followed by a retention test, in which physiological manipulations are presented. As in passive avoidance learning, food- or waterdeprived rats or mice finding food or water inside an enclosure are vulnerable to the retrograde amnesia produced by electroconvulsive shock treatment or the injection of various drugs. In one-trial taste or odor learning conducted in rats, birds, snails, bees, and fruit flies, there is an association between a food item or odorant and contextual stimuli or the unconditioned stimulus of Pavlovian conditioning. The odor-related task in bees was sensitive to protein synthesis inhibition as well as cholinergic receptor blockade, both analogous to results found on the passive avoidance response in rodents, while the task in fruit flies was sensitive to genetic modifications and aging, as seen in the passive avoidance response of genetically modified and aged rodents. These results provide converging evidence of interspecies similarities underlying the neurochemical basis of learning.

Keywords: Instrumental learning, pavlovian conditioning, food motivation, water motivation, electroconvulsive shock, cholinergic receptors, retrograde amnesia.

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[1]
Wang SH, Redondo RL, Morris RGM. Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci 2010; 107(45): 19537-42.
[http://dx.doi.org/10.1073/pnas.1008638107] [PMID: 20962282]
[2]
Sanford K, Clayton NS. Motivation and memory in zebra finch (Taeniopygia guttata) foraging behavior. Anim Cogn 2008; 11(2): 189-98.
[http://dx.doi.org/10.1007/s10071-007-0106-3] [PMID: 17891426]
[3]
Abreu F, Souto A, Schiel N. Wild common marmosets (Callithrix jacchus) employ spatial cognitive abilities to improve their food search and consumption: An experimental approach in small-scale space. Primates 2020; 61(6): 807-16.
[http://dx.doi.org/10.1007/s10329-020-00826-1] [PMID: 32383127]
[4]
Aggleton JP. One-trial object recognition by rats. Q J Exp Psychol B 1985; 37(4b): 279-94.
[http://dx.doi.org/10.1080/14640748508401171]
[5]
Mizunami M, Terao K, Alvarez B. Application of a prediction error theory to pavlovian conditioning in an insect. Front Psychol 2018; 9: 1272.
[http://dx.doi.org/10.3389/fpsyg.2018.01272] [PMID: 30083125]
[6]
Isaacson RL, Wickelgren WO. Hippocampal ablation and passive avoidance. Science 1962; 138(3545): 1104-6.
[http://dx.doi.org/10.1126/science.138.3545.1104] [PMID: 13956753]
[7]
Jarvik ME, Kopp R. An improved one-trial passive avoidance learning situation. Psychol Rep 1967; 21(1): 221-4.
[http://dx.doi.org/10.2466/pr0.1967.21.1.221] [PMID: 6078370]
[8]
Meyers B. Some effects of scopolamine on a passive avoidance response in rats. Psychopharmacology 1965; 8(2): 111-9.
[http://dx.doi.org/10.1007/BF00404171] [PMID: 5853734]
[9]
Tenen SS. Retrograde amnesia from electroconvulsive shock in a one-trial appetitive learning task. Science 1965; 148(3674): 1248-50.
[http://dx.doi.org/10.1126/science.148.3674.1248] [PMID: 14280014]
[10]
Anderson JE, Robichaud RC. Retrograde amnesia induced by hypoxia and electroconvulsive shock in two rat strains. Physiol Behav 1975; 14(1): 81-4.
[http://dx.doi.org/10.1016/0031-9384(75)90145-6] [PMID: 1171476]
[11]
Andrade C, Shaikh SA, Narayan L, Blasey C, Belanoff J. Administration of a selective glucocorticoid antagonist attenuates electroconvulsive shock-induced retrograde amnesia. J Neural Transm 2012; 119(3): 337-44.
[http://dx.doi.org/10.1007/s00702-011-0712-8] [PMID: 21922193]
[12]
Delprato DJ, Terrant FR Jr. Effect of ECS on passive avoidance learning with high and low intensity foot shock: Supplementary report. Psychol Rep 1966; 18(1): 121-2.
[http://dx.doi.org/10.2466/pr0.1966.18.1.121] [PMID: 5948586]
[13]
Mah CJ, Albert DJ. Reversal of ECS-induced amnesia by post-ECS injections of amphetamine. Pharmacol Biochem Behav 1975; 3(1): 1-5.
[http://dx.doi.org/10.1016/0091-3057(75)90072-6] [PMID: 1168925]
[14]
Quartermain D, McEwen BS, Azmitia EC Jr. Amnesia produced by electroconvulsive shock or cycloheximide: Conditions for recovery. Science 1970; 169(3946): 683-6.
[http://dx.doi.org/10.1126/science.169.3946.683] [PMID: 5464302]
[15]
Cahill L, McGaugh JL. Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav Neurosci 1990; 104(4): 532-43.
[http://dx.doi.org/10.1037/0735-7044.104.4.532] [PMID: 2206424]
[16]
Gold PE, Roberson NL, Delanoy RL. Post-training brain catecholamine levels: Lack of response to water-motivated training. Behav Neural Biol 1985; 44(3): 425-33.
[http://dx.doi.org/10.1016/S0163-1047(85)90808-8] [PMID: 4084187]
[17]
Pinel JP. A short gradient of ECS-produced amnesia in a one-trial appetitive learning situation. J Comp Physiol Psychol 1969; 68(4): 650-5.
[http://dx.doi.org/10.1037/h0027654] [PMID: 5388035]
[18]
Wansley RA, Holloway FA. Multiple retention deficits following one-trial appetitive training. Behav Biol 1975; 14(2): 135-49.
[http://dx.doi.org/10.1016/S0091-6773(75)90135-2] [PMID: 1137538]
[19]
Calhoun KS, Prewett MJ, Peters RD, Adams HE. Factors in the modification by isolation of electroconvulsive shock-produced retrograde amnesia in the rat. J Comp Physiol Psychol 1975; 88(1): 373-7.
[http://dx.doi.org/10.1037/h0076189] [PMID: 1168207]
[20]
Everett JC, Corson JA. ECS in one-trial appetitive learning of rats: Retention and amnesia. J Comp Physiol Psychol 1973; 84(2): 353-60.
[http://dx.doi.org/10.1037/h0035282] [PMID: 4737450]
[21]
White N, Major R, Siegel J. Effects of morphine on one-trial appetitive learning. Life Sci 1978; 23(19): 1967-71.
[http://dx.doi.org/10.1016/0024-3205(78)90564-7] [PMID: 723460]
[22]
Lalonde R, Vikis-Freibergs V. Manipulations of 5-HT activity and memory in the rat. Pharmacol Biochem Behav 1985; 22(3): 377-82.
[http://dx.doi.org/10.1016/0091-3057(85)90035-8] [PMID: 3873076]
[23]
Essman WB. Age dependent effects of 5-hydroxytryptamine upon memory consolidation and cerebral protein synthesis. Pharmacol Biochem Behav 1973; 1(1): 7-14.
[http://dx.doi.org/10.1016/0091-3057(73)90048-8] [PMID: 4775586]
[24]
Misane I, Ögren SO. Multiple 5-HT receptors in passive avoidance: Comparative studies of p-chloroamphetamine and 8-OH-DPAT. Neuropsychopharmacology 2000; 22(2): 168-90.
[http://dx.doi.org/10.1016/S0893-133X(99)00109-8] [PMID: 10649830]
[25]
Prado-Alcalá RA, Ruiloba MI, Rubio L, et al. Regional infusions of serotonin into the striatum and memory consolidation. Synapse 2003; 47(3): 169-75.
[http://dx.doi.org/10.1002/syn.10158] [PMID: 12494399]
[26]
Santucci AC, Knott PJ, Haroutunian V. Excessive serotonin release, not depletion, leads to memory impairments in rats. Eur J Pharmacol 1996; 295(1): 7-17.
[http://dx.doi.org/10.1016/0014-2999(95)00629-X] [PMID: 8925877]
[27]
Semba K, Adachi N, Arai T. Facilitation of serotonergic activity and amnesia in rats caused by intravenous anesthetics. Anesthesiology 2005; 102(3): 616-23.
[http://dx.doi.org/10.1097/00000542-200503000-00021] [PMID: 15731601]
[28]
Haapalinna A, Sirviö J, Lammintausta R. Facilitation of cognitive functions by a specific α2-adrenoceptor antagonist, atipamezole. Eur J Pharmacol 1998; 347(1): 29-40.
[http://dx.doi.org/10.1016/S0014-2999(98)00077-6] [PMID: 9650845]
[29]
Riekkinen P Jr, Sirviö J, Riekkinen M, Lammintausta R, Riekkinen P. Atipamezole, an α2 antagonist, stabilizes age-related high-voltage spindle and passive avoidance defects. Pharmacol Biochem Behav 1992; 41(3): 611-4.
[http://dx.doi.org/10.1016/0091-3057(92)90381-O] [PMID: 1350102]
[30]
Chopin P, Colpaert FC, Marien M. Effects of acute and subchronic administration of dexefaroxan, an alpha(2)-adrenoceptor antagonist, on memory performance in young adult and aged rodents. J Pharmacol Exp Ther 2002; 301(1): 187-96.
[http://dx.doi.org/10.1124/jpet.301.1.187] [PMID: 11907173]
[31]
Zarrindast MR, Ahmadi R, Oryan S, Parivar K, Haeri-Rohani A. Effects of α-adrenoceptor agonists and antagonists on histamine-induced impairment of memory retention of passive avoidance learning in rats. Eur J Pharmacol 2002; 454(2-3): 193-8.
[http://dx.doi.org/10.1016/S0014-2999(02)02497-4] [PMID: 12421647]
[32]
Barros DM, Izquierdo LA, Quevedo J, et al. Interaction between midazolam-induced anterograde amnesia and memory enhancement by treatments given hours later in hippocampus, entorrhinal cortex or posterior parietal cortex. Behav Pharmacol 1998; 9(2): 163-7.
[http://dx.doi.org/10.1097/00008877-200203000-00008] [PMID: 10065935]
[33]
Parkes SL, De la Cruz V, Bermúdez-Rattoni F, Coutureau E, Ferreira G. Differential role of insular cortex muscarinic and NMDA receptors in one-trial appetitive taste learning. Neurobiol Learn Mem 2014; 116: 112-6.
[http://dx.doi.org/10.1016/j.nlm.2014.09.008] [PMID: 25300672]
[34]
Petkov VV, Vuglenova Y. Pharmacological restoration of scopolamine-impaired memory. Acta Physiol Pharmacol Bulg 1985; 11(3): 37-43.
[PMID: 3938594]
[35]
Rush D. Reversal of scopolamine-induced amnesia of passive avoidance by pre- and post-training naloxone. Psychopharmacology 1986; 89(3): 296-300.
[http://dx.doi.org/10.1007/BF00174363] [PMID: 3088653]
[36]
Sullivan RM, Leon M. One-trial olfactory learning enhances olfactory bulb responses to an appetitive conditioned odor in 7-day-old rats. Brain Res Dev Brain Res 1987; 35(2): 307-11.
[http://dx.doi.org/10.1016/0165-3806(87)90056-3] [PMID: 3676845]
[37]
Noda A, Noda Y, Kamei H, et al. Phencyclidine impairs latent learning in mice: Interaction between glutamatergic systems and sigma(1) receptors. Neuropsychopharmacology 2001; 24(4): 451-60.
[http://dx.doi.org/10.1016/S0893-133X(00)00192-5] [PMID: 11182540]
[38]
Barber TA. Time course of memory formation for an appetitive, one-trial, water-reward task in day-old chicks. Behav Processes 2019; 158: 151-4.
[http://dx.doi.org/10.1016/j.beproc.2018.11.008] [PMID: 30458227]
[39]
Hilliard S, Nguyen M, Domjan M. One-trial appetitive conditioning in the sexual behavior system. Psychon Bull Rev 1997; 4(2): 237-41.
[http://dx.doi.org/10.3758/BF03209399] [PMID: 21331831]
[40]
Alexander J Jr, Audesirk TE, Audesirk GJ. One-trial reward learning in the snail Lymnea stagnalis. J Neurobiol 1984; 15(1): 67-72.
[http://dx.doi.org/10.1002/neu.480150107] [PMID: 6699634]
[41]
Kemenes I, Kemenes G, Andrew RJ, Benjamin PR, O’Shea M. Critical time-window for NO-cGMP-dependent long-term memory formation after one-trial appetitive conditioning. J Neurosci 2002; 22(4): 1414-25.
[http://dx.doi.org/10.1523/JNEUROSCI.22-04-01414.2002] [PMID: 11850468]
[42]
Fulton D, Kemenes I, Andrew RJ, Benjamin PR. A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning. Eur J Neurosci 2005; 21(5): 1347-58.
[http://dx.doi.org/10.1111/j.1460-9568.2005.03970.x] [PMID: 15813944]
[43]
Kuwabara M. Formation of the conditioned reflex of Pavlov's type in the honey bee, Apis mellifica. J Fac Sci Hokkaido Univ 1957; 13: 458-64.
[44]
Mercer AR, Menzel R. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 1982; 145(3): 363-8.
[http://dx.doi.org/10.1007/BF00619340]
[45]
Gauthier M, Cano-Lozano V, Zaoujal A, Richard D. Effects of intracranial injections of scopolamine on olfactory conditioning retrieval in the honeybee. Behav Brain Res 1994; 63(2): 145-9.
[http://dx.doi.org/10.1016/0166-4328(94)90085-X] [PMID: 7999297]
[46]
Biergans SD, Claudianos C, Reinhard J, Galizia CG. DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees. Front Mol Neurosci 2016; 9: 82.
[http://dx.doi.org/10.3389/fnmol.2016.00082] [PMID: 27672359]
[47]
Villar ME, Marchal P, Viola H, Giurfa M. Redefining single-trial memories in the honeybee. Cell Rep 2020; 30(8): 2603-13.
[http://dx.doi.org/10.1016/j.celrep.2020.01.086] [PMID: 32101739]
[48]
Lozano V, Armengaud C, Gauthier M. Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2001; 187(4): 249-54.
[http://dx.doi.org/10.1007/s003590100196] [PMID: 11467497]
[49]
Davis HP, Spanis CW, Squire LR. Inhibition of cerebral protein synthesis: Performance at different times after passive avoidance training. Pharmacol Biochem Behav 1976; 4(1): 13-6.
[http://dx.doi.org/10.1016/0091-3057(76)90168-4] [PMID: 1265091]
[50]
Flood JF, Bennett EL, Orme AE, Rosenzweig MR. Relation of memory formation to controlled amounts of brain protein synthesis. Physiol Behav 1975; 15(1): 97-102.
[http://dx.doi.org/10.1016/0031-9384(75)90285-1] [PMID: 1239025]
[51]
Wu LY, Chen WC, Tsai FS, Tsai CC, Wu CR, Lin LW. p-Hydroxybenzyl alcohol, an active phenolic ingredient of Gastrodia elata, reverses the cycloheximide-induced memory deficit by activating the adrenal gland in rats. Am J Chin Med 2015; 43(8): 1593-604.
[http://dx.doi.org/10.1142/S0192415X15500901] [PMID: 26621444]
[52]
Weiglein A, Gerstner F, Mancini N, Schleyer M, Gerber B. One-trial learning in larval Drosophila. Learn Mem 2019; 26(4): 109-20.
[http://dx.doi.org/10.1101/lm.049106.118] [PMID: 30898973]
[53]
König C, Gerber B. Age-related decrease in appetitive associative memory in fruit flies. J Exp Biol 2022; 225(21): jeb244915.
[http://dx.doi.org/10.1242/jeb.244915] [PMID: 36373856]
[54]
Bainbridge NK, Koselke LR, Jeon J, et al. Learning and memory impairments in a congenic C57BL/6 strain of mice that lacks the M2 muscarinic acetylcholine receptor subtype. Behav Brain Res 2008; 190(1): 50-8.
[http://dx.doi.org/10.1016/j.bbr.2008.02.001] [PMID: 18346798]
[55]
Marubio LM, Paylor R. Impaired passive avoidance learning in mice lacking central neuronal nicotinic acetylcholine receptors. Neuroscience 2004; 129(3): 575-82.
[http://dx.doi.org/10.1016/j.neuroscience.2004.09.003] [PMID: 15541879]
[56]
Tzavara ET, Bymaster FP, Felder CC, et al. Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiat 2003; 8(7): 673-9.
[http://dx.doi.org/10.1038/sj.mp.4001270] [PMID: 12874603]
[57]
Lamberty Y, Gower AJ. Age-related changes in spontaneous behavior and learning in NMRI mice from maturity to middle age. Physiol Behav 1990; 47(6): 1137-44.
[http://dx.doi.org/10.1016/0031-9384(90)90364-A] [PMID: 2395918]
[58]
Lippa A, Pelham R, Beer B, Critchett D, Dean R, Bartus R. Brain cholinergic dysfunction and memory in aged rats. Neurobiol Aging 1980; 1(1): 13-9.
[http://dx.doi.org/10.1016/0197-4580(80)90019-6] [PMID: 7266730]
[59]
Martinez JL Jr, Rigter H. Assessment of retention capacities in old rats. Behav Neural Biol 1983; 39(2): 181-91.
[http://dx.doi.org/10.1016/S0163-1047(83)90825-7] [PMID: 6670971]
[60]
Zornetzer SF, Thompson R, Rogers J. Rapid forgetting in aged rats. Behav Neural Biol 1982; 36(1): 49-60.
[http://dx.doi.org/10.1016/S0163-1047(82)90234-5] [PMID: 7168730]
[61]
Welsh KA, Gold PE. Brain catecholamines and memory modulation: Effects of footshock, amygdala implantation, and stimulation. Behav Neural Biol 1985; 43(2): 119-31.
[http://dx.doi.org/10.1016/S0163-1047(85)91317-2] [PMID: 4004685]
[62]
Femminella GD, Leosco D, Ferrara N, Rengo G. Adrenergic drugs blockers or enhancers for cognitive decline? What to choose for Alzheimer’s disease patients? CNS Neurol Disord Drug Targets 2016; 15(6): 665-71.
[http://dx.doi.org/10.2174/1871527315666160518123201] [PMID: 27189470]
[63]
Li S. The β‐adrenergic hypothesis of synaptic and microglial impairment in Alzheimer’s disease. J Neurochem 2023; 165(3): 289-302.
[http://dx.doi.org/10.1111/jnc.15782] [PMID: 36799441]
[64]
Tampi RR, Tampi DJ, Farheen SA, Ochije SI, Joshi P. Propranolol for the management of behavioural and psychological symptoms of dementia. Drugs Context 2022; 11(11): 1-11.
[http://dx.doi.org/10.7573/dic.2022-8-3] [PMID: 36544625]
[65]
Beracochea D. Anterograde and retrograde effects of benzodiazepines on memory. Sci World J 2006; 6: 1460-5.
[http://dx.doi.org/10.1100/tsw.2006.243] [PMID: 17115086]
[66]
McNamara RK, Skelton RW. Diazepam impairs acquisition but not performance in the morris water maze. Pharmacol Biochem Behav 1991; 38(3): 651-8.
[http://dx.doi.org/10.1016/0091-3057(91)90028-Z] [PMID: 2068203]
[67]
Bauer PJ, Leventon JS, Varga NL. Neuropsychological assessment of memory in preschoolers. Neuropsychol Rev 2012; 22(4): 414-24.
[http://dx.doi.org/10.1007/s11065-012-9219-9] [PMID: 23143341]
[68]
Deshpande A, Van Boekholt B, Zuberbuhler K. Preliminary evidence for one-trial social learning of vervet monkey alarm calling. R Soc Open Sci 2022; 9(8): 210560.
[http://dx.doi.org/10.1098/rsos.210560] [PMID: 36016915]
[69]
Ferrucci L, Nougaret S, Genovesio A. Macaque monkeys learn by observation in the ghost display condition in the object-in-place task with differential reward to the observer. Sci Rep 2019; 9(1): 401.
[http://dx.doi.org/10.1038/s41598-018-36803-4] [PMID: 30674953]

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