Neuronal generator patterns at scalp elicited by lateralized aversive pictures reveal consecutive stages of motivated attention

Jürgen Kayser1,2, Craig E. Tenke1,2, Karen S. Abraham1, Daniel M. Alschuler1, Jorge E. Alvarenga1, Jamie Skipper3, Virginia Warner3,4, Gerard E. Bruder1,2, Myrna M. Weissman2,3,4

1Division of Cognitive Neuroscience, New York State Psychiatric Institute, New York, NY, USA; 2Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USA; 3Division of Epidemiology, New York State Psychiatric Institute, New York, NY, USA; 4Mailman School of Public Health, Columbia University, New York, NY, USA

Received 2 March 2016; revised 21 April 2016; accepted 24 May 2016; published online 2 June 2016.

Abstract

Event-related potential (ERP) studies have provided evidence for an allocation of attentional resources to enhance perceptual processing of motivationally salient stimuli. Emotional modulation affects several consecutive components associated with stages of affective-cognitive processing, beginning as early as 100-200 ms after stimulus onset. In agreement with the notion that the right parietotemporal region is critically involved during the perception of arousing affective stimuli, some ERP studies have reported asymmetric emotional ERP effects. However, it is difficult to separate emotional from non-emotional effects because differences in stimulus content unrelated to affective salience or task demands may also be associated with lateralized function or promote cognitive processing. Other concerns pertain to the operational definition and statistical independence of ERP component measures, their dependence on an EEG reference, and spatial smearing due to volume conduction, all of which impede the identification of distinct scalp activation patterns associated with affective processing. Building on prior research using a visual half-field paradigm with highly-controlled emotional stimuli (pictures of cosmetic surgery patients showing disordered [negative] or healed [neutral] facial areas before or after treatment), 72-channel ERPs recorded from 152 individuals (age 13-68 years; 81 female) were transformed into reference-free current source density (CSD) waveforms and submitted to temporal principal components analysis (PCA) to identify their underlying neuronal generator patterns. Using both nonparametric randomization tests and repeated measures ANOVA, robust effects of emotional content were found over parietooccipital regions for CSD factors corresponding to N2 sink (212 ms peak latency), P3 source (385 ms) and a late centroparietal source (630 ms), all indicative of greater positivity for negative than neutral stimuli. For N2 sink, emotional effects were right-lateralized and modulated by hemifield, with larger amplitude and asymmetry for left hemifield (right hemisphere) presentations. For all three factors, more positive amplitudes at parietooccipital sites were associated with increased ratings of negative valence and greater arousal. Distributed inverse solutions of the CSD-PCA-based emotional effects implicated a sequence of maximal activations in right occipitotemporal cortex, bilateral posterior cingulate cortex and bilateral inferior temporal cortex. These findings are consistent with hierarchical activations of the ventral visual pathway reflecting subsequent processing stages in response to motivationally salient stimuli.

Key Words: Event-related potential (ERP); Current source density (CSD); Principal components analysis (PCA); Source localization; Late positive potential (LPP); Emotional lateralization

doi:10.1016/j.neuroimage.2016.05.059