Working memory capacity is associated with optimal adaptation of response bias to perceptual sensitivity in emotion perception

Emotion perception, inferring the emotional state of another person, is a frequent judgment made under perceptual uncertainty (e.g., a scowling facial expression can indicate anger or concentration) and behavioral risk (e.g., incorrect judgment can be costly to the perceiver). Working memory capacity (WMC), the ability to maintain controlled processing in the face of competing demands, is an important component of many decisions. We investigated the association of WMC and anger perception in a task in which “angry” and “not angry” categories comprised overlapping ranges of scowl intensity, and correct and incorrect responses earned and lost points, respectively. Participants attempted to earn as many points as they could; adopting an optimal response bias would maximize decision utility. Participants with higher WMC more optimally tuned their anger perception response bias to accommodate their perceptual sensitivity (their ability to discriminate the categories) than did participants with lower WMC. Other factors that influence response bias (i.e., the relative base rate of angry vs. not angry faces and the decision costs & benefits) were ruled out as contributors to the WMC- bias relationship. Our results suggest that WMC optimizes emotion perception by contributing to perceivers’ ability to adjust their response bias to account for their level of perceptual sensitivity, likely an important component of adapting emotion perception to dynamic social interactions and changing circumstances.

Lynn, S. K., Ibagon, C., Bui, E., Palitz, S., Simon, N. M., & Barrett, L. F. (2016). Working memory capacity is associated with optimal adaptation of response bias to perceptual sensitivity in emotion perception. Emotion 16(2):155-163.

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Decision making from economic and signal detection perspectives: Development of an integrated framework

Behavior is comprised of decisions made from moment to moment (i.e., to respond one way or another). Often, the decision maker cannot be certain of the value to be accrued from the decision (i.e., the outcome value). Decisions made under outcome value uncertainty form the basis of the economic framework of decision making. Behavior is also based on perception — perception of the external physical world and of the internal bodily milieu, which both provide cues that guide decision making. These perceptual signals are also often uncertain: another person’s scowling facial expression may indicate threat or intense concentration, alternatives that require different responses from the perceiver. Decisions made under perceptual uncertainty form the basis of the signals framework of decision making. Traditional behavioral economic approaches to decision making focus on the uncertainty that comes from variability in possible outcome values, and typically ignore the influence of perceptual uncertainty. Conversely, traditional signal detection approaches to decision making focus on the uncertainty that arises from variability in perceptual signals and typically ignore the influence of outcome value uncertainty. Here, we compare and contrast the economic and signals frameworks that guide research in decision making, with the aim of promoting their integration. We show that an integrated framework can expand our ability to understand a wider variety of decision- making behaviors, in particular the complexly determined real-world decisions we all make every day.

Lynn, S. K.*, Wormwood, J.B.*, Barrett, L. F., & Quigley, K. S. (In press). Decision making from economic and signal detection perspectives: Development of an integrated framework. Frontiers in Psychology. DOI: 10.3389/fpsyg.2015.00952.

*These authors contributed equally to the study.

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“Utilizing” signal detection theory

What do inferring what a person is thinking or feeling, judging a defendant’s guilt, and navigating a dimly lit room have in common? They involve perceptual uncertainty (e.g., a scowling face might indicate anger or concentration, for which different responses are appropriate) and behavioral risk (e.g., a cost to making the wrong response). Signal detection theory describes these types of decisions. In this tutorial, we show how incorporating the economic concept of utility allows signal detection theory to serve as a model of optimal decision making, going beyond its common use as an analytic method. This utility approach to signal detection theory clarifies otherwise enigmatic influences of perceptual uncertainty on measures of decision-making performance (accuracy and optimality) and on behavior (an inverse relationship between bias magnitude and sensitivity optimizes utility). A “utilized” signal detection theory offers the possibility of expanding the phenomena that can be understood within a decision-making framework.

Lynn, S.K, and L.F. Barrett. 2014. “Utilizing” signal detection theory. Psychological Science, 25(9):1663–1673.

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Gender differences in oxytocin-associated disruption of decision bias during emotion perception

Oxytocin is associated with differences in the perception of and response to socially mediated information, such as facial expressions. Across studies, however, oxytocin’s effect on emotion perception has been inconsistent. Outside the laboratory, emotion perception involves interpretation of perceptual uncertainty and assessment of behavioral risk. An account of these factors is largely missing from studies of oxytocin’s effect on emotion perception and might explain inconsistent results across studies. Of relevance, studies of oxytocin’s effect on learning and decision-making indicate that oxytocin attenuates risk aversion. We used the probability of encountering angry faces and the cost of misidentifying them as not angry to create a risky environment wherein bias to categorize faces as angry would maximize point earnings. Consistent with an underestimation of the factors creating risk (i.e., encounter rate and cost), men given oxytocin exhibited a worse (i.e., less liberal) response bias than men given placebo. Oxytocin did not influence women’s performance. These results suggest that oxytocin may impair men’s ability to adapt to changes in risk and uncertainty when introduced to novel or changing social environments. Because oxytocin also influences behavior in non-social realms, oxytocin pharmacotherapy could have unintended consequences (i.e., risk-prone decision-making) while nonetheless normalizing pathological social interaction.

Lynn, S. K.*, Hoge, E. A.*, Fischer, L. E., Barrett, L. F., and Simon, N. M. 2014. Gender differences in oxytocin-associated disruption of decision bias during emotion perception. Psychiatry Research 219, 198-203. DOI:10.1016/j.psychres.2014.04.031

*These authors contributed equally to the study.

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These data also presented at ACNP 2012 and CNS 2013.

Affective state influences perception by affecting decision parameters underlying bias and sensitivity

Studies of the effect of affect on perception often show consistent directional effects of a person’s affective state on perception. Unpleasant emotions have been associated with a “locally focused” style of stimulus evaluation, and positive emotions with a “globally focused” style. Typically, however, studies of affect and perception have not been conducted under the conditions of perceptual uncertainty and behavioral risk inherent to perceptual judgments outside the laboratory. We investigated the influence of perceivers’ experienced affect (valence and arousal) on the utility of social threat perception by combining signal detection theory and behavioral economics. We compared 3 perceptual decision environments that systematically differed with respect to factors that underlie uncertainty and risk: the base rate of threat, the costs of incorrect identification threat, and the perceptual similarity of threats and nonthreats. We found that no single affective state yielded the best performance on the threat perception task across the 3 environments. Unpleasant valence promoted calibration of response bias to base rate and costs, high arousal promoted calibration of perceptual sensitivity to perceptual similarity, and low arousal was associated with an optimal adjustment of bias to sensitivity. However, the strength of these associations was conditional upon the difficulty of attaining optimal bias and high sensitivity, such that the effect of the perceiver’s affective state on perception differed with the cause and/or level of uncertainty and risk.

Lynn, SK, X Zhang, & LF Barrett. 2012. Affective state influences perception by affecting decision parameters underlying bias and sensitivity. Emotion 12(4):726-736.

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Behavioral effects of clozapine: Involvement of trace amine pathways in C. elegans and M. musculus

Clozapine is an antipsychotic medication with superior efficacy in treatment refractory schizophrenia. The molecular basis of clozapine’s therapeutic profile is not well understood. We studied behavioral effects of clozapine in Caenorhabditis elegans to identify novel pathways that modulate clozapine’s biological effects. Clozapine stimulated egg laying in C. elegans in a dose-dependent manner. This effect was clozapine-specific, as it was not observed with exposure to a typical antipsychotic, haloperidol or an atypical antipsychotic, olanzapine. A candidate gene screen of biogenic amine neurotransmitter systems identified signaling pathways that mediate this clozapine-specific effect on egg laying. Specifically, we found that clozapine-induced increase in egg laying requires tyramine biosynthesis. To test the implications of this finding across species, we explored whether trace amine systems modulate clozapine’s behavioral effects in mammals by studying trace amine-associated receptor 1 (TAAR1) knockout mice. Clozapine increased prepulse inhibition (PPI) in wild-type mice. This increase in PPI was abrogated in TAAR1 knockout mice, implicating TAAR1 in clozapine-induced PPI enhancement. In transfected mammalian cell lines, we found no TAAR activation by antipsychotics, suggesting that modulation of trace amine signaling in mice does not occur directly at the receptor itself. In summary, we report a heretofore- unknown role for trace amine systems in clozapine-mediated effects across two species: C. elegans and mice.

Karmacharya, R.*, S.K. Lynn*, S. Demarco, A. Ortiz, X. Wang, M.Y. Lundy, Z. Xie, B.M. Cohen, G.M. Miller, and E.A. Buttner. 2011. Behavioral effects of clozapine: Involvement of trace amine pathways in C. elegans and M. musculus. Brain Research 1393:91-99.

* These authors contributed equally to the study.

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Decision-Making and Learning: The Peak Shift Behavioral Response

[Excerpt] Peak shift is taxonomically widespread: exhibited by birds; mammals, including humans; fish; and at least some arthropods. The phenomenon thus appears to reflect uni- versal attributes of generalization, discrimination learning, and choice-making behavior. As such, peak shift is a ‘model’ type of decision making, suitable for comparative study at functional and mechanistic levels. Using peak shift as a tractable example of decision making, a variety of organisms can be studied, with strengths differentially well suited to phylogenetic, behavioral, neural, cellular, or molecular investigations.

In addition to being well suited to study at multiple levels, considerations of peak shift go beyond what is typically investigated in research on decision making. Many models of behavioral economics maximize utility: these models consider variability in (1) the costs and benefits of obtaining resources, and how those payoffs change with body state, and (2) the probability of encountering resources of some quality. Game theoretic approaches additionally account for the effect of others’ responses on the decision maker’s own behavior. However, these models overlook the fact that an animal’s estimates of a resource’s payoff and probability are based on sensory signals emitted by the resource. Outside of the laboratory, signals, such as color or tail length, vary. This variation may exist indepen- dently of any variation in the information encoded by the signals. For example, a signal that indicates a particular food quality (yellow skin on a banana signals ripeness) may vary even if the food quality itself does not (ten bananas of the same ripeness may not share the same yellow color). Typical utility optimization approaches account for variance in resource quality, not variance in the stimuli that signal that quality. Since real world signals are noisy, our understanding of choice behavior will be incomplete with- out accounting for signal variation and uncertainty. As a signal detection issue, peak shift experiments present an opportunity to investigate the role of this signal-borne risk in decision making and its interactions with those aspects of decision making more commonly investigated.

Lynn, S.K. 2010. Decision-making and learning: The peak shift behavioral response. In M. Breed & J. Moore (Eds.), Encyclopedia of Animal Behavior (Vol. 1, pp. 470-475). Oxford: Academic Press. DOI: 10.1016/B978-0-08-045337-8.00146-7

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Normal thermoregulatory responses to 3-iodothyronamine, trace amines and amphetamine-like psychostimulants in trace amine associated receptor 1 knockout mice

3-Iodothyronamine (T1AM) is a metabolite of thyroid hor- mone. It is an agonist at trace amine-associated receptor 1 (TAAR1), a recently identified receptor involved in mono- aminergic regulation and a potential novel therapeutic tar- get. Here, T1AM was studied using rhesus monkey TAAR1 and/or human dopamine transporter (DAT) co- transfected cells, and wild-type (WT) and TAAR1 knock- out (KO) mice. The IC50 of T1AM competition for binding of the DAT-specific radio-ligand [3H]CFT was highly similar in DAT cells, WT striatal synaptosomes and KO striatal synaptosomes (0.72–0.81 lM). T1AM inhibition of 10 nM [3H]dopamine uptake (IC50: WT, 1.4 6 0.5 lM; KO, 1.2 6 0.4 lM) or 50 nM [3H]serotonin uptake (IC50: WT, 4.5 6 0.6 lM; KO, 4.7 6 1.1 lM) in WT and KO synaptosomes was also highly similar. Unlike other TAAR1 agonists that are DAT substrates, TAAR1 signaling in response to T1AM was not enhanced in the presence of DAT as determined by CRE-luciferase assay. In vivo, T1AM induced robust hypothermia in WT and KO mice equivalently and dose dependently (maximum change degrees Celsius: 50 mg/ kg at 60 min: WT 26.0 6 0.4, KO 25.6 6 1.0; and 25 mg/kg at 30 min: WT 22.7 6 0.4, KO 23.0 6 0.2). Other TAAR1 agonists including beta–phenylethylamine (b-PEA), MDMA (3,4-methylenedioxymethamphetamine) and meth- amphetamine also induced significant, time-dependent thermoregulatory responses that were alike in WT and KO mice. Therefore, TAAR1 co-expression does not alter T1AM binding to DAT in vitro nor T1AM inhibition of [3H]monoamine uptake ex vivo, and TAAR1 agonist- induced thermoregulatory responses are TAAR1-inde- pendent. Accordingly, TAAR1-directed compounds will likely not affect thermoregulation nor are they likely to be cryogens.

Panas, HN, LJ Lynch, EJ Vallender, Z Xie, G Chen, SK Lynn, TS Scanlan, and GM Miller. 2010. Normal thermoregulatory responses to 3-iodothyronamine, trace amines and amphetamine-like psychostimulants in trace amine associated receptor 1 knockout mice. Journal of Neuroscience Research 88:1962-2969.

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Neurophysiological correlates of comprehending emotional meaning in context

Although the neurocognitive mechanisms of nonaffective language comprehension have been studied extensively, relatively less is known about how the emotional meaning of language is processed. In this study, electrophysiological responses to affectively positive, negative, and neutral words, presented within nonconstraining, neutral contexts, were evaluated under conditions of explicit evaluation of emotional content (Experiment 1) and passive reading (Experiment 2). In both experiments, a widely distributed Late Positivity was found to be larger to negative than to positive words (a ‘‘negativity bias’’). In addition, in Experiment 2, a small, posterior N400 effect to negative and positive (relative to neutral) words was detected, with no differences found between N400 magnitudes to negative and positive words. Taken together, these results suggest that comprehending the emotional meaning of words following a neutral context requires an initial semantic analysis that is relatively more engaged for emotional than for nonemotional words, whereas a later, more extended, attention-modulated process distinguishes the specific emotional valence (positive vs. negative) of words. Thus, emotional processing networks within the brain appear to exert a continuous influence, evident at several stages, on the construction of the emotional meaning of language.

Holt, D.J., S.K. Lynn, and G.R. Kuperberg. 2009. Neurophysiological correlates of comprehending emotional meaning in context. Journal of Cognitive Neuroscience.

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Attenuated modulation of the N170 ERP by facial expressions in schizophrenia

In psychiatrically-well subjects the modulation of event related potentials (ERPs) by emotional facial expressions is found in several ERPs from ~100 ms and later. A face-related EPR, the N170, is abnormally reduced in schizophrenia to faces relative to other complex objects and research suggests emotional modulation of N170 may be reduced as well. To further examine facial emotion modulation of N170, subjects detected neutral facial expressions from among five emotional expressions (happy, sad, fearful, angry, and disgusted). Over occipitotemporal sites, psychiatrically-well subjects showed bilateral differences in N170 amplitude among expressions (P=0.014). Schizophrenia subjects failed to show this modulation (P=0.551). Accuracy on the task did not differ between groups, nor did the pattern of errors. However, in patients, greater positive and negative symptom ratings were associated with increased failure to button press to neutral faces, suggesting misattribution of emotion to neutral expressions in the more ill patients. Because the N170 is largely specific to faces, these results suggest that an impairment specific to the visual processing of facial expressions contributes to the well-known behavioral abnormalities in facial emotion tasks in schizophrenia.

Lynn, S.K., and D.F. Salisbury. 2008. Attenuated modulation of the N170 ERP by facial expressions in schizophrenia. Journal of Clinical EEG & Neuroscience 39(2):108-111.

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