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Norepinephrine Ignites Local Hotspots of Neuronal Excitation: How Arousal Amplifies Selectivity in Perception and Memory

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Norepinephrine Ignites Local Hotspots of Neuronal Excitation: How Arousal Amplifies Selectivity in Perception and Memory BEHAVIORAL AND BRAIN SCIENCES (2016), Page 1 of 75 doi:10.1017/S0140525X15000667, e200 Norepinephrine ignites local hotspots of neuronal excitation: How arousal amplifies selectivity in perception and memory Mara Mather Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089-0191 [email protected] David Clewett Neuroscience Graduate Program, University of Southern California, Los Angeles, CA 90089-2520 [email protected] Michiko Sakaki School of Psychology and Clinical Language Sciences, University of Reading, Reading RGX 7BE, United Kingdom; and Kochi University of Technology, Kami, 782-0003, Japan [email protected] Carolyn W. Harley Professor Emeritus, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, Canada [email protected] Abstract: Emotional arousal enhances perception and memory of high-priority information but impairs processing of other information. Here, we propose that, under arousal, local glutamate levels signal the current strength of a representation and interact with norepinephrine (NE) to enhance high priority representations and out-compete or suppress lower priority representations. In our "glutamate amplifies noradrenergic effects" (GANE) model, high glutamate at the site of prioritized representations increases local NE release from the locus coeruleus (LC) to generate “NE hotspots.” At these NE hotspots, local glutamate and NE release are mutually enhancing and amplify activation of prioritized representations. In contrast, arousal-induced LC activity inhibits less active representations via two mechanisms: 1) Where there are hotspots, lateral inhibition is amplified; 2) Where no hotspots emerge, NE levels are only high enough to activate low-threshold inhibitory adrenoreceptors. Thus, LC activation promotes a few hotspots of excitation in the context of widespread suppression, enhancing high priority representations while suppressing the rest. Hotspots also help synchronize oscillations across neural ensembles transmitting high-priority information. Furthermore, brain structures that detect stimulus priority interact with phasic NE release to preferentially route such information through large-scale functional brain networks. A surge of NE before, during, or after encoding enhances synaptic plasticity at NE hotspots, triggering local protein synthesis processes that enhance selective memory consolidation. Together, these noradrenergic mechanisms promote selective attention and memory under arousal. GANE not only reconciles apparently contradictory findings in the emotion-cognition literature but also extends previous influential theories of LC neuromodulation by proposing specific mechanisms for how LC-NE activity increases neural gain. Keywords: arousal; attention; emotion; locus coeruleus; long-term consolidation; memory; norepinephrine; perception 1. Introduction information and less on peripheral information (Easterbrook 1959). Since his seminal paper, researchers have accumulated When jolted by a rough skydiving landing, psychologist James many more observations that arousal evoked by emotional Easterbrook observed that his sense of space and time shrank events enhances some aspects of perception and memory and slowly re-expanded (Easterbrook 1982). This sparked his but impairs others (for reviews, see Mather & Sutherland curiosity about how arousal influences attention. Later he 2011; Reisberg & Heuer 2004). For example, victims of a published a review article in which he argued that under crime tend to remember the weapon vividly but forget the arousal, people rely more on central or immediately relevant perpetrator’s face (Steblay 1992). People also pay attention © Cambridge University Press 2016 0140-525X/16 Downloaded from https://www.cambridge.org/core. Graduate Institute, on 30 May 2018 at 11:35:20, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms1 . https://doi.org/10.1017/S0140525X15001879 Mather et al.: Norepinephrine ignites local hotspots of neuronal excitation to emotional information at the expense of neutral informa- Bottom-up processes are largely automatic, determined tion (Dolcos & McCarthy 2006; Knight et al. 2007). These by the perceptual properties of a stimulus, and do not examples fit with Easterbrook’s formulation that arousal depend on top-down attention or task demands. For impairs attention to peripheral information. But arousing example, stimuli that contrast with their surroundings, stimuli can sometimes enhance memory of peripheral such as a bright light in a dark room, engage attention auto- neutral information (Kensinger et al. 2007; Knight & matically even if they are currently goal irrelevant (Itti & Mather 2009). Thus, although it is clear that arousal Koch 2000; Parkhurst et al. 2002; Reynolds & Desimone shapes attention and memory, knowing that something is 2003). Top-down goals can also bias competition in favor neutral or spatially peripheral is not enough to predict of particular stimuli that otherwise would not stand out. how it will fare under emotional conditions. Although not included in the original biased competition So, then, how does arousal influence the brain’s selection models, past history with particular stimuli is also a of features to highlight versus suppress? An initial answer to source of selection bias (Awh et al. 2012; Hutchinson & this puzzle was provided by the arousal-biased competi- Turk-Browne 2012). For example, one’s name or a novel tion (ABC) model, which posits that arousal does not have stimulus tends to engage attention (Moray 1959; Reicher fixed rules about which types of stimuli to enhance or et al. 1976). In addition, faces, text, and emotionally suppress. Instead, arousal amplifies the stakes of ongoing salient stimuli all grab attention (e.g., Cerf et al. 2009; selection processes, leading to “winner-take-more” and Knight et al. 2007; MacKay et al. 2004; Niu et al. 2012). “loser-take-less” effects in perception and memory (Mather A core aspect of most current theories of visual attention is & Sutherland 2011). The ABC model builds on biased com- that these different signals are integrated into maps of the petition models proposing that stimuli must compete for environment that indicate the priority or salience of stimuli limited mental resources (Beck & Kastner 2009; Desimone across different locations (Itti & Koch 2000; Soltani & & Duncan 1995; Duncan 2006). As conceptualized by Desi- Koch 2010;Treisman1998). Regions in frontoparietal mone and Duncan (1995), both bottom-up and top-down cortex integrating sensory and top-down signals help repre- neural mechanisms help resolve competition. sent such priority maps (Ptak 2012). Moreover, having both feedforward and feedback connections between sensory regions and cortical priority maps enables distributed repre- sentations of prioritized information to modulate their own DAVID CLEWETT, who received his Ph.D. in Neurosci- processing (e.g., lower-level visual features) even further ence, has been the recipient of two Endowed Fellow- (Klink et al. 2014;Ptak2012; Serences & Yantis 2007; ships from the University of Southern California. His Soltani & Koch 2010). Thus, priority signals are self-biasing research focuses on the role of the noradrenergic fi system in mediating the influence of arousal on to enhance ef cient information processing in the brain. memory and healthy cognitive aging. In 2014, he was In the ABC model, arousal further biases mental process- recognized as the program’s Neuroscience Student of ing to favor high- over low-priority representations, regard- the Year. less of whether initial priority is determined by bottom-up salience, emotional salience, or top-down goals. Thus, CAROLYN HARLEY, Professor Emeritus in Psychology because spatially peripheral information is usually lower pri- and Neuroscience at Memorial University of New- ority than central information, arousal usually impairs foundland, is the author of more than 95 publications memory for it (Steblay 1992; Waring & Kensinger 2011). in learning and memory and brain plasticity with a Yet, when peripheral information is perceptually salient special focus on norepinephrine and the locus coeru- or goal relevant, arousal instead enhances memory for it leus. She has served as President of the Canadian Society for Brain, Behavior and Cognitive Science. (e.g., Kensinger et al. 2007, Experiment 4). But the ABC Her ongoing research program is concerned with model does not tackle how this works in the brain. Previous behavioral functions of noradrenergic locus coeruleus brain-based models of emotion and cognition also do not activation and is funded by the Natural Sciences and account for the dual role of arousal. Most models posit Engineering Research Council of Canada. that the amygdala enhances perception and memory consolidation of emotionally salient stimuli, but fail to MARA MATHER, Professor of Gerontology and Psychol- address how arousal sometimes enhances and sometimes ogy at the University of Southern California, conducts – impairs information processing. research focusing on emotion cognition interactions In this article we propose the glutamate amplifies nor- with a particular focus on how emotional arousal adrenergic effects (GANE) model, in which arousal shapes perception and memory. She has received the fi Distinguished Scientific Award for Early Career Contri- ampli es the activation difference between high- and low-priority representations via local synaptic self-regulation bution to Psychology from the
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