Locus Coeruleus Activity Strengthens Prioritized Memories Under Arousal

被引:101
作者
Clewett, David V. [1 ]
Huang, Ringo [2 ]
Velasco, Rico [2 ]
Lee, Tae-Ho [3 ]
Mather, Mara [1 ,2 ]
机构
[1] Univ Southern Calif, Neurosci Grad Program, 3715 McClintock Ave,Room 351, Los Angeles, CA 90089 USA
[2] Univ Southern Calif, Davis Sch Gerontol, Los Angeles, CA 90089 USA
[3] Univ N Carolina, Dept Psychol & Neurosci, Chapel Hill, NC 27599 USA
基金
美国国家卫生研究院;
关键词
emotion; locus ceruleus; memory; motivation; norepinephrine; pupil; MEDIAL TEMPORAL-LOBE; INDEPENDENT COMPONENT ANALYSIS; EMOTIONAL MEMORY; PUPIL-DILATION; NORADRENERGIC MODULATION; BIASED COMPETITION; COGNITIVE RESERVE; LASTING MEMORIES; SUBSTANTIA-NIGRA; MRI CONTRAST;
D O I
10.1523/JNEUROSCI.2097-17.2017
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Recent models posit that bursts of locus ceruleus (LC) activity amplify neural gain such that limited attention and encoding resources focus even more on prioritized mental representations under arousal. Here, we tested this hypothesis in human males and females using fMRI, neuromelanin MRI, and pupil dilation, a biomarker of arousal and LC activity. During scanning, participants performed a monetary incentive encoding task in which threat of punishment motivated them to prioritize encoding of scene images over superimposed objects. Threat of punishment elicited arousal and selectively enhanced memory for goal-relevant scenes. Furthermore, trial-level pupil dilations predicted better scene memory under threat, but were not related to object memory outcomes. fMRI analyses revealed that greater threat-evoked pupil dilations were positively associated with greater scene encoding activity in LC and parahippocampal cortex, a region specialized to process scene information. Across participants, this pattern of LC engagement for goal-relevant encoding was correlated with neuromelanin signal intensity, providing the first evidence that LC structure relates to its activation pattern during cognitive processing. Threat also reduced dynamic functional connectivity between high-priority (parahippocampal place area) and lower-priority (lateral occipital cortex) category-selective visual cortex in ways that predicted increased memory selectivity. Together, these findings support the idea that, under arousal, LC activity selectively strengthens prioritized memory representations by modulating local and functional network-level patterns of information processing.
引用
收藏
页码:1558 / 1574
页数:17
相关论文
共 102 条
[1]   Reward-motivated learning: Mesolimbic activation precedes memory formation [J].
Adcock, R. Alison ;
Thangavel, Arul ;
Whitfield-Gabrieli, Susan ;
Knutson, Brian ;
Gabrieli, John D. E. .
NEURON, 2006, 50 (03) :507-517
[2]   Pupil size signals mental effort deployed during multiple object tracking and predicts brain activity in the dorsal attention network and the locus coeruleus [J].
Alnaes, Dag ;
Sneve, Markus Handal ;
Espeseth, Thomas ;
Endestad, Tor ;
de Pavert, Steven Harry Pieter Van ;
Laeng, Bruno .
JOURNAL OF VISION, 2014, 14 (04)
[3]   Emotion enhances remembrance of neutral events past [J].
Anderson, AK ;
Wais, PE ;
Gabrieli, JDE .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (05) :1599-1604
[4]  
[Anonymous], 2007, Technical report B-3
[5]  
[Anonymous], 2001, FUNCT MRI INTRO METH
[6]   Eyes wide open: enhanced pupil dilation when selectively studying important information [J].
Ariel, Robert ;
Castel, Alan D. .
EXPERIMENTAL BRAIN RESEARCH, 2014, 232 (01) :337-344
[7]   Comment on "Modafinil Shifts Human Locus Coeruleus to Low-Tonic, High-Phasic Activity During Functional MRI" and "Homeostatic Sleep Pressure and Responses to Sustained Attention in the Suprachiasmatic Area" [J].
Astafiev, Serguei V. ;
Snyder, Abraham Z. ;
Shulman, Gordon L. ;
Corbetta, Maurizio .
SCIENCE, 2010, 328 (5976)
[8]   Role of locus coeruleus in attention and behavioral flexibility [J].
Aston-Jones, G ;
Rajkowski, J ;
Cohen, J .
BIOLOGICAL PSYCHIATRY, 1999, 46 (09) :1309-1320
[9]   An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance [J].
Aston-Jones, G ;
Cohen, JD .
ANNUAL REVIEW OF NEUROSCIENCE, 2005, 28 :403-450
[10]   Mixed-effects modeling with crossed random effects for subjects and items [J].
Baayen, R. H. ;
Davidson, D. J. ;
Bates, D. M. .
JOURNAL OF MEMORY AND LANGUAGE, 2008, 59 (04) :390-412