Awareness of Emotional Expressions in Cannabis Users : An Event-Related Potential Study

Robert D. Torrence, Donald C. Rojas and Lucy J. Troup

Frontiers in Psychology, February 2019 | Volume 10 | Article 69

ORIGINAL RESEARCH

doi: 10.3389/fpsyg.2019.00069

Abstract

Cannabis use has been associated with anxiogenic effects when used in low frequency for a short duration, but cannabis can also have anxiogenic effects when used heavily for a long duration. Animal studies have indicated the neurobiological mechanisms related to cannabis and anxiety; however, research has been limited on the related neurocognitive mechanisms. Previous research has indicated that cannabis use is associated with alterations in event-related potentials (ERPs). The purpose of the current study was to examine anxiety related attentional processing of emotional expressions using ERP methods. We used a backward masking paradigm to restrict awareness of facial expressions (i.e., fearful, happy, and neutral). The results indicated that cannabis use was associated with differences in emotional processing. Specifically, the results suggested cannabis users had increased P1 amplitudes toward happy facial expressions compared to fearful and neutral. Additionally, cannabis users seemed to have reduced N170 hemisphere lateralization.

Keywords : cannabis, ERP, emotion, facial expression, awareness

INTRODUCTION

There has been a significant increase in cannabis use among adolescents between 2002 and 2015 (Substance Abuse and Mental Health Services Administration, 2016). Given that cannabis use has increased in availability and use, likely because of the increased legalization in the United States (National Conference of State Legislatures, 2018), it is important to understand the effects cannabis use has on the brain and behavior. Previous research has suggested that cannabis use was correlated with decreased memory, attention, and emotional processing (Broyd et al., 2016; Troup et al., 2016b, 2017; Lovell et al., 2018). Neuroanatomical differences have also been found between cannabis users and non-users: specifically in the amygdala, prefrontal cortex (PFC), and insula (Lorenzetti et al., 2016). The endocannabinoid system has been a target for treatment of anxiety related disorders (Rabinak and Phan, 2014; Korem et al., 2016); however, how cannabis might affect emotion processing is unclear. The main phytocannabinoid found in cannabis, 19-tetrahydrocannabinol (THC), has been suggested to have anxiolytic effects (Berrendero and Maldonado, 2002; Viveros et al., 2005; Patel and Hillard, 2006; Rubino et al., 2007), although other research has indicated that excessive cannabis use has anxiogenic effects (Viveros et al., 2005). Individuals with anxiety tend to have enhanced attention and processing
of threat-related (Bar-Haim et al., 2007) and positive (Morel et al., 2014) stimuli. These differences in attentional processing can be measured using event-related potentials (ERPs) (Harrewijn et al., 2017). The aim of this study was to examine the residual effects of cannabis use on attention to emotional facial expressions when awareness was restricted, versus when awareness was not restricted using a backward masking paradigm.

Backward masking occurs when a target face is displayed for a short duration and then is immediately replaced by a mask stimulus (neutral face or scrambled face). Pessoa et al. (2005) conducted a behavioral study in which they varied the target face (fearful, happy, or neutral face) and target duration (17, 33, and 83 ms) to test the awareness threshold duration for the target face. The researchers found that a target face duration of 17 ms was below the awareness threshold for most of the participants (nine out of 11); at 33 ms, seven out of 11 participants scored above chance level in detecting the target face, and all of the participants were aware of the target face displayed for 83 ms. These results suggested there are individual differences in perceptual awareness and established that backward masking is most effective when the target faces are displayed for 17 ms or less.

Backward masking fMRI studies suggested the amygdala was more active for negative facial expressions compared with neutral or happy faces, even when awareness was restricted (Morris et al., 1998; Whalen et al., 1998; Suslow et al., 2006). Similarly, dot-probe task fMRI research found that the visual cortex had increased activity when attending toward fearful faces (Pourtois et al., 2006; Carlson et al., 2011), and visual cortex activity was correlated with amygdala activity (Carlson et al., 2009). Researchers have used ERPs to measure the time-course of processing facial expressions. A number of studies indicated that even when awareness of emotional facial expressions was restricted using backward masking, multiple ERP components were modulated by negative target faces (fear and anger) compared to non-negative faces (happy and neutral) (Pegna et al., 2008, 2011; Del Zotto and Pegna, 2015; Vukusic et al., 2017). The P1 ERP component has a positive peak around 80–120 ms in the lateral occipital electrodes. Participants with high trait anxiety had more enhanced P1 amplitude to happy faces compared to neutral, and there was no difference between fear and neutral (Morel et al., 2014); whereas other research suggested that P1 was more enhanced in high anxiety toward negative stimuli (Helfinstein et al., 2008; Holmes et al., 2008; Mueller et al., 2009; Harrewijn et al., 2017; Torrence and Troup, 2017). Overall the P1 component is thought to reflect an initial increase of attention in the extrastriate cortex (Mangun et al., 1997; Pourtois et al., 2005) and is more pronounced in anxiety. The N170 component is a negative deflection in the ERP waveform which peaks around 170 ms after stimulus onset and is found in lateral posterior electrodes, which typically has a right hemisphere lateralization (Bentin et al., 1996). A meta-analysis indicated that the N170 is sensitive to facial expression: particularly to anger, fear, and happiness expressions (Hinojosa et al., 2015). In addition, these studies found that the overall amplitude of N170 was more negative for faces displayed for a long duration compared to a short duration. That is, when awareness of a fearful face was restricted, the N170 was enhanced compared to neutral. The same was found when awareness was not restricted, but the amplitude in the aware condition was more negative overall. Source localization of the N170 was found to originate in the right extrastriate visual cortex (Pegna et al., 2008). However, another study indicated that emotional expression did not influence the N170 (Kiss and Eimer, 2008).

In addition to P1 and N170, the N2 component has also been suggested to indicate orientation to salient facial expressions regardless of awareness (Liddell et al., 2004; Vukusic et al., 2017). The N2 ERP component is the second negative peak occurring 180–300 ms and can be found in central electrodes (i.e., FZ, CZ, and PZ). Contrary to Liddell et al. (2004) and Pegna et al. (2008), Vukusic et al. (2017) only found N2 differences in unmasked conditions as opposed to masked. Other research suggested the N2 component involves cognitive control, or controlling actions (Folstein and Van Petten, 2008). Although the source of anterior N2 is debated, it is thought to originate in the medial frontal cortex (e.g., ACC) and the right inferior frontal cortex (Ridderinkhof and Ullsperger, 2004; Folstein and Van Petten, 2008; Aron et al., 2016). Lastly, the P3 ERP component has multiple subcomponents, but this article focuses on the later P3 between 400 and 600 ms found in central, posterior electrodes (Kiss and Eimer, 2008). The enhanced P3 amplitude reflects higher level emotional and attentional processing (Johnston et al., 1986; Polich, 2007). Previous research suggested that cannabis use modulates the P3 amplitude toward emotional facial expressions, particularly in implicitly processed (Troup et al., 2016b, 2017).

The main purpose of this study was to examine the residual effects of cannabis use on processing facial expression under restricted awareness. Given the relationship between awareness and processing of emotional expressions and anxiety, as well as the effects cannabis has on anxiety, we hypothesized that individuals that use cannabis would have residual attenuation in their ERPs in responses to emotional faces (similar to what researchers have found in low anxiety). More specifically, cannabis users would have reduced (less enhanced) P1, N170, N2, and P3 amplitudes to fearful and happy facial expression. These results would indicate that processing of emotional expressions could be a neutral cognitive mechanism of the anxiolytic effects of cannabis use.

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