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The International Journal on the Biology of Stress
Volume 24, 2021 - Issue 2: Commemorating the 2nd Munich Stress Conference
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Short Communications

Noradrenergic enhancement of object recognition and object location memory in mice

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Pages 181-188 | Received 28 Oct 2019, Accepted 19 Mar 2020, Published online: 11 Apr 2020

References

  • Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28(1), 403–450. doi:10.1146/annurev.neuro.28.061604.135709
  • Atucha, E., Vukojevic, V., Fornari, R. V., Ronzoni, G., Demougin, P., Peter, F., Atsak, P., Coolen, M. W., Papassotiropoulos, A., McGaugh, J. L., de Quervain, D. J.-F., & Roozendaal, B. (2017). Noradrenergic activation of the basolateral amygdala maintains hippocampus-dependent accuracy of remote memory. Proceedings of the National Academy of Sciences, 114(34), 9176–9181. doi:10.1073/pnas.1710819114
  • Balderas, I., Rodriguez-Ortiz, C. J., Salgado-Tonda, P., Chavez-Hurtado, J., Mcgaugh, J. L., & Bermudez-Rattoni, F. (2008). The consolidation of object and context recognition memory involve different regions of the temporal lobe. Learning & Memory, 15(9), 618–624. doi:10.1101/lm.1028008
  • Barker, G. R., & Warburton, E. C. (2011). When is the hippocampus involved in recognition memory? Journal of Neuroscience, 31(29), 10721–10731.
  • Barsegyan, A., McGaugh, J. L., & Roozendaal, B. (2014). Noradrenergic activation of the basolateral amygdala modulates the consolidation of object-in-context recognition memory. Frontiers in Behavioral Neuroscience, 8, 160. doi:10.3389/fnbeh.2014.00160
  • Barsegyan, A., Mirone, G., Ronzoni, G., Guo, C., Song, Q., van Kuppeveld, D., Schut, E. H. S., Atsak, P., Teurlings, S., McGaugh, J. L., Schubert, D., & Roozendaal, B. (2019). Glucocorticoid enhancement of recognition memory via basolateral amygdala-driven facilitation of prelimbic cortex interactions. Proceedings of the National Academy of Sciences, 116(14), 7077–7082. doi:10.1073/pnas.1901513116
  • Beldjoud, H., Barsegyan, A., & Roozendaal, B. (2015). Noradrenergic activation of the basolateral amygdala enhances object recognition memory and induces chromatin remodeling in the insular cortex. Frontiers in Behavioral Neuroscience, 9(108), 108. doi:10.3389/fnbeh.2015.00108
  • Berman, D. E., Hazvi, S., Neduva, V., & Dudai, Y. (2000). The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: Activation of erk1–2 and formation of a memory trace. The Journal of Neuroscience, 20(18), 7017–7023. doi:10.1523/JNEUROSCI.20-18-07017.2000
  • Bevilaqua, L., Ardenghi, P., Shröder, N., Bromberg, E., Schmitz, P., Schaeffer, E., Quevedo, J., Bianchin, M., Walz, R., & Medina, J. (1997). Drugs acting upon the cyclic adenosine monophosphate/protein kinase a signalling pathway modulate memory consolidation when given late after training into rat hippocampus but not amygdala. Behavioural Pharmacology, 8(4), 331–338.
  • Bianchi, M., Fone, K., Azmi, N., Heidbreder, C., Hagan, J., & Marsden, C. (2006). Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. European Journal of Neuroscience, 24(10), 2894–2902. doi:10.1111/j.1460-9568.2006.05170.x
  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198. doi:10.1038/nrn2575
  • Cahill, L., Gorski, L., & Le, K. (2003). Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning & Memory, 10(4), 270–274. doi:10.1101/lm.62403
  • Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994). Β-adrenergic activation and memory for emotional events. Nature, 371(6499), 702–704. doi:10.1038/371702a0
  • Chen, Y., Barsegyan, A., Nadif Kasri, N., & Roozendaal, B. (2018). Basolateral amygdala noradrenergic activity is required for enhancement of object recognition memory by histone deacetylase inhibition in the anterior insular cortex. Neuropharmacology, 141, 32–41. doi:10.1016/j.neuropharm.2018.08.018
  • Costa-Miserachs, D., Portell-Cortés, I., Aldavert-Vera, L., Torras-García, M., & Morgado-Bernal, I. (1994). Long-term memory facilitation in rats by posttraining epinephrine. Behavioral Neuroscience, 108(3), 469–474. doi:10.1037/0735-7044.108.3.469
  • Coutellier, L., & Würbel, H. (2009). Early environmental cues affect object recognition memory in adult female but not male c57bl/6 mice. Behavioural Brain Research, 203(2), 312–315. doi:10.1016/j.bbr.2009.05.001
  • Do Nascimento, E. B., Dierschnabel, A. L., de Macêdo Medeiros, A., Suchecki, D., Silva, R. H., & Ribeiro, A. M. (2019). Memory impairment induced by different types of prolonged stress is dependent on the phase of the estrous cycle in female rats. Hormones and Behavior, 115, 104563. doi:10.1016/j.yhbeh.2019.104563
  • Dornelles, A., de Lima, M. N., Grazziotin, M., Presti-Torres, J., Garcia, V. A., Scalco, F. S., Roesler, R., & Schroder, N. (2007). Adrenergic enhancement of consolidation of object recognition memory. Neurobiology of Learning and Memory, 88(1), 137–142. doi:10.1016/j.nlm.2007.01.005
  • Ferry, B., & McGaugh, J. L. (1999). Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiology of Learning and Memory, 72(1), 8–12. doi:10.1006/nlme.1998.3904
  • Gold, P. E., & Van Buskirk, R. B. (1975). Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behavioral Biology, 13(2), 145–153. doi:10.1016/S0091-6773(75)91784-8
  • Graham, B. M., & Scott, E. (2018). Effects of systemic estradiol on fear extinction in female rats are dependent on interactions between dose, estrous phase, and endogenous estradiol levels. Hormones and Behavior, 97, 67–74. doi:10.1016/j.yhbeh.2017.10.009
  • Hatfield, T., & McGaugh, J. L. (1999). Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of Learning and Memory, 71(2), 232–239. doi:10.1006/nlme.1998.3875
  • Hermans, E. J., Battaglia, F. P., Atsak, P., de Voogd, L. D., Fernandez, G., & Roozendaal, B. (2014). How the amygdala affects emotional memory by altering brain network properties. Neurobiology of Learning and Memory, 112, 2–16. doi:10.1016/j.nlm.2014.02.005
  • Hermans, E. J., Henckens, M. J., Joels, M., & Fernandez, G. (2014). Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends in Neurosciences, 37(6), 304–314. doi:10.1016/j.tins.2014.03.006
  • Hermans, E. J., van Marle, H. J. F., Ossewaarde, L., Henckens, M. J. A. G., Qin, S., van Kesteren, M. T. R., Schoots, V. C., Cousijn, H., Rijpkema, M., Oostenveld, R., & Fernandez, G. (2011). Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science, 334(6059), 1151–1153. doi:10.1126/science.1209603
  • Hok, V., Poucet, B., Duvelle, E., Save, E., & Sargolini, F. (2016). Spatial cognition in mice and rats: Similarities and differences in brain and behavior. Wiley Interdisciplinary Reviews: Cognitive Science, 7(6), 406–421. doi:10.1002/wcs.1411
  • Introini-Collison, I. B., & McGaugh, J. L. (1986). Epinephrine modulates long-term retention of an aversively motivated discrimination. Behavioral and Neural Biology, 45(3), 358–365. doi:10.1016/S0163-1047(86)80024-3
  • Introini-Collison, I. B., Miyazaki, B., & McGaugh, J. L. (1991). Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology, 104(4), 541–544. doi:10.1007/BF02245663
  • Izquierdo, I., & Dias, R. D. (1985). Influence on memory of posttraining or pre-test injections of acth, vasopressin, epinephrine, and β-endorphin, and their interaction with naloxone. Psychoneuroendocrinology, 10(2), 165–172. doi:10.1016/0306-4530(85)90054-X
  • Jurado-Berbel, P., Costa-Miserachs, D., Torras-Garcia, M., Coll-Andreu, M., & Portell-Cortes, I. (2010). Standard object recognition memory and “what” and “where” components: Improvement by post-training epinephrine in highly habituated rats. Behavioural Brain Research, 207(1), 44–50. doi:10.1016/j.bbr.2009.09.036
  • Kirry, A. J., Durigan, D. J., Twining, R. C., & Gilmartin, M. R. (2019). Estrous cycle stage gates sex differences in prefrontal muscarinic control of fear memory formation. Neurobiology of Learning and Memory, 161, 26–36. doi:10.1016/j.nlm.2019.03.001
  • Laing, M., & Bashir, Z. (2014). Β-adrenoceptors and synaptic plasticity in the perirhinal cortex. Neuroscience, 273, 163–173. doi:10.1016/j.neuroscience.2014.04.070
  • LaLumiere, R. T., Buen, T.-V., & McGaugh, J. L. (2003). Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. The Journal of Neuroscience, 23(17), 6754–6758. doi:10.1523/JNEUROSCI.23-17-06754.2003
  • Leger, M., Quiedeville, A., Bouet, V., Haelewyn, B., Boulouard, M., Schumann-Bard, P., & Freret, T. (2013). Object recognition test in mice. Nature Protocols, 8(12), 2531–2537. doi:10.1038/nprot.2013.155
  • Li, J.-T., Su, Y.-A., Guo, C.-M., Feng, Y., Yang, Y., Huang, R.-H., & Si, T.-M. (2011). Persisting cognitive deficits induced by low-dose, subchronic treatment with mk-801 in adolescent rats. European Journal of Pharmacology, 652(1–3), 65–72. doi:10.1016/j.ejphar.2010.10.074
  • Liang, K. C., Juler, R. G., & McGaugh, J. L. (1986). Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research, 368(1), 125–133. doi:10.1016/0006-8993(86)91049-8
  • Liang, K., McGaugh, J. L., & Yao, H.-Y. (1990). Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Research, 508(2), 225–233. doi:10.1016/0006-8993(90)90400-6
  • Luine, V. (2002). Sex differences in chronic stress effects on memory in rats. Stress, 5(3), 205–216. doi:10.1080/1025389021000010549
  • McGaugh, J. L. (2000). Memory–a century of consolidation. Science, 287(5451), 248–251. doi:10.1126/science.287.5451.248
  • McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27(1), 1–28. doi:10.1146/annurev.neuro.27.070203.144157
  • McIntyre, C. K., Hatfield, T., & McGaugh, J. L. (2002). Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. European Journal of Neuroscience, 16(7), 1223–1226. doi:10.1046/j.1460-9568.2002.02188.x
  • McIntyre, C. K., Miyashita, T., Setlow, B., Marjon, K. D., Steward, O., Guzowski, J. F., & McGaugh, J. L. (2005). Memory-influencing intra-basolateral amygdala drug infusions modulate expression of arc protein in the hippocampus. Proceedings of the National Academy of Sciences, 102(30), 10718–10723. doi:10.1073/pnas.0504436102
  • McReynolds, J. R., Anderson, K. M., Donowho, K. M., & McIntyre, C. K. (2014). Noradrenergic actions in the basolateral complex of the amygdala modulate arc expression in hippocampal synapses and consolidation of aversive and non-aversive memory. Neurobiology of Learning and Memory, 115, 49–57. doi:10.1016/j.nlm.2014.08.016
  • Minni, A., de Medeiros, G., Helbling, J.-C., Duittoz, A., Marissal-Arvy, N., Foury, A., De Smedt-Peyrusse, V., Pallet, V., & Moisan, M.-P. (2014). Role of corticosteroid binding globulin in emotional reactivity sex differences in mice. Psychoneuroendocrinology, 50, 252–263. doi:10.1016/j.psyneuen.2014.07.029
  • Murty, V. P., Ritchey, M., Adcock, R. A., & LaBar, K. S. (2010). Fmri studies of successful emotional memory encoding: A quantitative meta-analysis. Neuropsychologia, 48(12), 3459–3469. doi:10.1016/j.neuropsychologia.2010.07.030
  • Nirogi, R., Abraham, R., Jayarajan, P., Medapati, R. B., Shanmuganathan, D., Kandikere, V., Irappanavar, S., Saralaya, R., Benade, V., Bhyrapuneni, G., & Muddana, N. (2012). Difference in the norepinephrine levels of experimental and non-experimental rats with age in the object recognition task. Brain Research, 1453, 40–45. doi:10.1016/j.brainres.2012.03.013
  • O’Carroll, R. E., Drysdale, E., Cahill, L., Shajahan, P., & Ebmeier, K. P. (1999). Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material in man. Psychological Medicine, 29(5), 1083–1088. doi:10.1017/S0033291799008703
  • Okuda, S., Roozendaal, B., & McGaugh, J. L. (2004). Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences, 101(3), 853–858. doi:10.1073/pnas.0307803100
  • Pezze, M. A., Marshall, H. J., Fone, K. C., & Cassaday, H. J. (2017). Role of the anterior cingulate cortex in the retrieval of novel object recognition memory after a long delay. Learning & Memory, 24(7), 310–317. doi:10.1101/lm.044784.116
  • Quirarte, G. L., Galvez, R., Roozendaal, B., & McGaugh, J. L. (1998). Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs. Brain Research, 808(2), 134–140. doi:10.1016/S0006-8993(98)00795-1
  • Roozendaal, B., Castello, N. A., Vedana, G., Barsegyan, A., & McGaugh, J. L. (2008). Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory. Neurobiology of Learning and Memory, 90(3), 576–579. doi:10.1016/j.nlm.2008.06.010
  • Roozendaal, B., Hernandez, A., Cabrera, S. M., Hagewoud, R., Malvaez, M., Stefanko, D. P., Haettig, J., & Wood, M. A. (2010). Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. Journal of Neuroscience, 30(14), 5037–5046. doi:10.1523/JNEUROSCI.5717-09.2010
  • Roozendaal, B., & McGaugh, J. L. (2011). Memory modulation. Behavioral Neuroscience, 125(6), 797–824. doi:10.1037/a0026187
  • Roozendaal, B., Nguyen, B. T., Power, A. E., & McGaugh, J. L. (1999). Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences, 96(20), 11642–11647. doi:10.1073/pnas.96.20.11642
  • Roozendaal, B., Okuda, S., Van der Zee, E. A., & McGaugh, J. L. (2006). Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences, 103(17), 6741–6746.
  • Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10(3), 211–223. doi:10.1038/nrn2573
  • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., & Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27(9), 2349–2356. doi:10.1523/JNEUROSCI.5587-06.2007
  • Southwick, S. M., Davis, M., Horner, B., Cahill, L., Morgan, C. A., III, Gold, P. E., Bremner, J. D., & Charney, D. C. (2002). Relationship of enhanced norepinephrine activity during memory consolidation to enhanced long-term memory in humans. American Journal of Psychiatry, 159(8), 1420–1422. doi:10.1176/appi.ajp.159.8.1420
  • Stefanko, D. P., Barrett, R. M., Ly, A. R., Reolon, G. K., & Wood, M. A. (2009). Modulation of long-term memory for object recognition via hdac inhibition. Proceedings of the National Academy of Sciences, 106(23), 9447–9452. doi:10.1073/pnas.0903964106
  • Stepanichev, M., Markov, D., Pasikova, N., & Gulyaeva, N. (2016). Behavior and the cholinergic parameters in olfactory bulbectomized female rodents: Difference between rats and mice. Behavioural Brain Research, 297, 5–14. doi:10.1016/j.bbr.2015.09.033
  • Sternberg, D., Isaacs, K., Gold, P. E., & McGaugh, J. (1985). Epinephrine facilitation of appetitive learning: Attenuation with adrenergic receptor antagonists. Behavioral and Neural Biology, 44(3), 447–453. doi:10.1016/S0163-1047(85)90856-8
  • Sutcliffe, J., Marshall, K., & Neill, J. (2007). Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behavioural Brain Research, 177(1), 117–125. doi:10.1016/j.bbr.2006.10.029
  • Szemeredi, K., Komoly, S., Kopin, I. J., Bagdy, G., Keiser, H. R., & Goldstein, D. S. (1991). Simultaneous measurement of plasma and brain extracellular fluid concentrations of catechols after yohimbine administration in rats. Brain Research, 542(1), 8–14. doi:10.1016/0006-8993(91)90990-D
  • Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernandez, G., Deisseroth, K., Greene, R. W., & Morris, R. G. (2016). Locus coeruleus and dopaminergic consolidation of everyday memory. Nature, 537(7620), 357–362. doi:10.1038/nature19325
  • Van Den Heuvel, M. P., & Pol, H. E. H. (2010). Exploring the brain network: A review on resting-state fmri functional connectivity. European Neuropsychopharmacology, 20(8), 519–534. doi:10.1016/j.euroneuro.2010.03.008
  • Van Leeuwen, J., Vink, M., Fernández, G., Hermans, E., Joëls, M., Kahn, R., & Vinkers, C. (2018). At-risk individuals display altered brain activity following stress. Neuropsychopharmacology, 43(9), 1954–1960. doi:10.1038/s41386-018-0026-8
  • Vogel-Ciernia, A., & Wood, M. A. (2014). Examining object location and object recognition memory in mice. Current Protocols in Neuroscience, 69(1), 17–31. 8.31doi:10.1002/0471142301.ns0831s69
  • Wimmer, M. E., Hernandez, P. J., Blackwell, J., & Abel, T. (2012). Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiology of Aging, 33(9), 2220–2224. doi:10.1016/j.neurobiolaging.2011.07.007
  • Zerbi, V., Floriou-Servou, A., Markicevic, M., Vermeiren, Y., Sturman, O., Privitera, M., von Ziegler, L., Ferrari, K. D., Weber, B., De Deyn, P. P., Wenderoth, N., & Bohacek, J. (2019). Rapid reconfiguration of the functional connectome after chemogenetic locus coeruleus activation. Neuron, 103(4), 702–718 e705. doi:10.1016/j.neuron.2019.05.034