Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T22:28:26.202Z Has data issue: false hasContentIssue false
  • English
  • Français

Importance of amygdala noradrenergic activity and large-scale neural networks in regulating emotional arousal effects on perception and memory1

Published online by Cambridge University Press:  05 January 2017

Benno Roozendaal ,
Laura Luyten ,
Lycia D. de Voogd  and
Erno J. Hermans
Benno Roozendaal
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, 6500 HB Nijmegen, The [email protected] Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The [email protected]@donders.ru.nlhttp://www.ru.nl/donders/research/theme-3-plasticity/
Laura Luyten
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, 6500 HB Nijmegen, The [email protected] Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The [email protected]@donders.ru.nlhttp://www.ru.nl/donders/research/theme-3-plasticity/ Center for the Psychology of Learning and Experimental Psychopathology, KU Leuven, 3000 Leuven, [email protected]
Lycia D. de Voogd
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, 6500 HB Nijmegen, The [email protected] Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The [email protected]@donders.ru.nlhttp://www.ru.nl/donders/research/theme-3-plasticity/
Erno J. Hermans
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, 6500 HB Nijmegen, The [email protected] Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The [email protected]@donders.ru.nlhttp://www.ru.nl/donders/research/theme-3-plasticity/
Get access Rights & Permissions [Opens in a new window]

Abstract

Mather and colleagues postulate that norepinephrine promotes selective processing of emotionally salient information through local “hotspots” where norepinephrine release interacts with glutamatergic activity. However, findings in rodents and humans indicate that norepinephrine is ineffective in modulating mnemonic processes in the absence of a functional amygdala. We therefore argue that emphasis should shift toward modulatory effects of amygdala-driven changes at the network level.

Type
Open Peer Commentary
Information
Behavioral and Brain Sciences , Volume 39 , 2016 , e222
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1.

BR and LL contributed equally to the preparation of this commentary.

References

Abercrombie, H. C., Speck, N. S. & Monticelli, R. M. (2006) Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused. Psychoneuroendocrinology 31(2):187–96.CrossRefGoogle ScholarPubMed
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:Article 160.CrossRefGoogle ScholarPubMed
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C. & Damasio, A. R. (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269(5227):1115–18.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Bennion, K. A., Ford, J. H., Murray, B. D. & Kensinger, E. A. (2013) Oversimplification in the study of emotional memory. Journal of the International Neuropsychological Society 19(9):953–61.Google Scholar
Cahill, L., Babinsky, R., Markowitsch, H. J. & McGaugh, J. L. (1995) The amygdala and emotional memory. Nature 377(6547):295–96.CrossRefGoogle ScholarPubMed
Cahill, L., Prins, B., Weber, M. & McGaugh, J. L. (1994) Beta-adrenergic activation and memory for emotional events. Nature 371(6499):702–704.Google Scholar
Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D. & Cahill, L. (2000) Event-related activation in the human amygdala associates with later memory for individual emotional experience. The Journal of Neuroscience 20(19):RC99.CrossRefGoogle ScholarPubMed
Dolcos, F., LaBar, K. S. & Cabeza, R. (2004) Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42(5):855–63.CrossRefGoogle ScholarPubMed
Fastenrath, M., Coynel, D., Spalek, K., Spalek, K., Milnik, A., Gschwind, L., Roozendaal, B., Papassotiropoulos, A. & de Quervain, J. F. (2014) Dynamic modulation of amygdala–hippocampal connectivity by emotional arousal. The Journal of Neuroscience 34(42):13935–47.Google Scholar
Ghosh, S. & Chattarji, S. (2015) Neuronal encoding of the switch from specific to generalized fear. Nature Neuroscience 18(1):112–20.Google Scholar
Hamann, S. B., Ely, T. D., Grafton, S. T. & Kilts, C. D. (1999) Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience 2(3):289–93.CrossRefGoogle ScholarPubMed
Hermans, E. J., Battaglia, F. P., Atsak, P., de Voogd, L. D., Fernández, G. & Roozendaal, B. (2014) How the amygdala affects emotional memory by altering brain network properties. Neurobiology of Learning and Memory 112:2–16.Google Scholar
Hermans, E. J., van Marle, H. J. F., Ossewaarde, L., Henckens, M., Qin, S. Z., 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):1151–53. doi: 10.1126/science.1209603.CrossRefGoogle ScholarPubMed
Klumpers, F., Morgan, B., Terburg, D., Stein, D. J. & van Honk, J. (2014) Impaired acquisition of classically conditioned fear-potentiated startle reflexes in humans with focal bilateral basolateral amygdala damage. Social Cognitive and Affective Neuroscience 10(9):1161–68.Google Scholar
Kuhlmann, S. & Wolf, O. T. (2006) Arousal and cortisol interact in modulating memory consolidation in healthy young men. Behavioral Neuroscience 120(1):217–23.CrossRefGoogle ScholarPubMed
Lovitz, E. S. & Thompson, L. T. (2015) Memory-enhancing intra-basolateral amygdala clenbuterol infusion reduces post-burst afterhyperpolarizations in hippocampal CA1 pyramidal neurons following inhibitory avoidance learning. Neurobiology of Learning and Memory 119(1):34–41.CrossRefGoogle ScholarPubMed
Mather, M. & Sutherland, M. R. (2011) Arousal-biased competition in perception and memory. Perspectives on Psychological Science 6(2):114–33. doi: 10.1177/1745691611400234.Google Scholar
McGaugh, J. L. (2002) Memory consolidation and the amygdala: A systems perspective. Trends in Neuroscience 25(9):456–61.CrossRefGoogle ScholarPubMed
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 of the United States of America 102(30):10718–23.CrossRefGoogle ScholarPubMed
Quirarte, G. L., Roozendaal, B. & McGaugh, J. L. (1997) Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 94(25):14048–53.Google Scholar
Richardson, M. P., Strange, B. A. & Dolan, R. J. (2004) Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience 7(3):278–85.CrossRefGoogle ScholarPubMed
Roozendaal, B. & McGaugh, J. L. (2011) Memory modulation. Behavioral Neuroscience 125(6):797–824. doi: 10.1037/a0026187.CrossRefGoogle ScholarPubMed
Roozendaal, B., Nguyen, B. T., Power, A. E. & McGaugh, J. L. (1999) Basolateral amygdala noradrenergic influence on the memory-enhancing effect of glucocorticoid receptor activation in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 96(20):11642–47.Google Scholar
Strange, B. A. & Dolan, R. J. (2004) Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proceedings of the National Academy of Sciences of the United States of America 101(31):11454–58.CrossRefGoogle ScholarPubMed
Strange, B. A., Hurlemann, R. & Dolan, R. J. (2003) An emotion-induced retrograde amnesia in humans is amygdala- and beta-adrenergic-dependent. Proceedings of the National Academy of Sciences of the United States of America 100(23):13626–31. Available at: http://www.ncbi.nlm.nih.gov/pubmed/14595032.Google Scholar
Terburg, D., Morgan, B. E., Montoya, E. R., Hooge, I. T., Thornton, H. B., Hariri, A. R. Panksepp, J., Stein, D. J. & van Honk, J. (2012) Hypervigilance for fear after basolateral amygdala damage in humans. Translational Psychiatry 2:e115.Google Scholar
Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J. & Dolan, R. J. (2004) Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neuroscience 7(11):1271–78.Google Scholar