Emotional arousal amplifies competitions across goal-relevant representation: A neurocomputational framework

Abstract

Emotional arousal often facilitates memory for some aspects of an event while impairing memory for other aspects of the same event. Across three experiments, we found that emotional arousal amplifies competition among goal-relevant representations, such that arousal impairs memory for multiple goal-relevant representations while enhancing memory for solo goal-relevant information. We also present a computational model to explain the mechanisms by which emotional arousal can modulate memory in opposite ways via the local/synaptic-level noradrenergic system. The model is based on neurophysiological observations that norepinephrine (NE) released under emotional arousal is locally controlled by glutamate levels, resulting in different NE effects across regions, gating either long-term potentiation or long-term depression by activating different adrenergic receptors depending on NE concentration levels. This model successfully replicated behavioral findings from the three experiments. These findings suggest that the NE's local effects are key in determining the effects of emotion on memory.

Keywords: Emotion and memory; Neural network model; Norepinephrine; Retrograde amnesia.

Figure 1.

Procedures in experiments. (A) In the conditioning phase, participants learned associations between a neutral tone and electric stimulation (CS+) and associations between another tone and lack of stimulation (CS−). (B) During the learning phase in Studies 1 and 2, participants learned four faces in the multiple condition or one face in the solo condition, followed by CS+ or CS−. Face images were taken from the TarrLab face database for illustration purpose only (stimulus images courtesy of Michael J. Tarr, Center for the Neural Basis of Cognition, Carnegie Mellon University, http://www.tarrlab.org).

Figure 2.

Results from Studies 1 and 2. (A–B) CS+ induced higher SCRs than did CS− during the conditioning phase. (C–D) During the final memory test, there were selective impairment effects of emotional arousal on memory in the multiple condition. Error bars represent standard errors of means.

Figure 3.

Results from the working memory test in Studies 1 (A) and 2 (B). Error bars represent standard errors of means.

Figure 4.

Procedures in the learning phase in Study 3. Participants learned four objects in the multiple condition and one face in the solo condition, while faces in the solo condition were preceded by cues and highlighted to enhance their priority. Face images were taken from the TarrLab face database for illustration purpose only (stimulus images courtesy of Michael J. Tarr, Center for the Neural Basis of Cognition, Carnegie Mellon University, http://www.tarrlab.org).

Figure 5.

Results from Study 3. (A) CS+ induced higher SCRs than did CS− during the conditioning phase. (B) During the final memory test, emotion enhanced memory for solo high-priority faces. (C) Performance in the working memory test. Error bars represent standard errors of means.

Figure 6.

A schematic representation of our neural network model. The figure displays only two of the input and output units for simplicity.

Figure 7.

Simulation results for the arousal-induced competition. (A) The model showed that arousal enhances memory in the solo condition but impairs memory in the multiple condition. The model also reproduced the weaker enhancement effects of arousal observed in Studies 1 and 2. Data were averaged across 20 simulations. Error bars represent standard errors. (B) The results from our three studies were summarized to make it easier to compare the results from our simulation and psychological data.

Figure 8.

Local NE values in the output unit during the learning phase in (A) the solo condition, (B) the multiple condition (here we present the averaged NE values over four items) and (C) the multiple condition (separately for strongly activated items and weakly activated items). To illustrate the threshold to activate β receptors (a solid line) and the threshold to activate α1 receptors (a gray dashed line), raw NE values were log-transformed after converting them into nMol and shown in the figures. Data from one of the 20 simulations.

Figure 9.

The model’s behavior and its fit with behavioral data when changing key parameters for GANE. Data were averaged across 20 simulations.

Figure 10.

The potential factors that determine signal strength of high-priority target representations and affect whether the item shows facilitative or impairing effects of arousal.