CommentaryWhat does the prefrontal cortex “do” in affect: perspectives on frontal EEG asymmetry research
Introduction
It is very gratifying for me personally to be writing this commentary since the publication of this Special Issue marks the fact that there now exists a substantial corpus of scientific literature investigating methodological and conceptual issues surrounding the use of measures of asymmetric prefrontal electrical signals recorded from the scalp surface to make inferences about emotional processes. With my colleagues and students at the time, I first reported 25 years ago on the use of asymmetries in scalp-recorded frontal brain electrical activity to make inferences about emotional processes (Davidson et al., 1979). At the time, it was a lonely field though there were investigators from other domains of neuroscience who underscored the important role played by the prefrontal cortex in different aspects of emotional processes (e.g., Nauta, 1971). This Special Issue has brought together the best of current research using these non-invasive measures to investigate different aspects of the methodology and construct validity of these measures. When I began to work in this area, research on the central nervous system substrates of emotional processes was largely restricted to studies in non-human species that focused on the role of subcortical structures in emotional and motivational processes, leading to a view, still championed by some (e.g., Panksepp, 2003; but see Davidson, 2003a for a rebuttal), that the fundamental circuitry for emotion and motivation lies in subcortical zones and that cortical tissue has little if anything directly to do with emotion. The only exceptions to this view at the time came from observations of patients with localized cortical brain damage (e.g., Gainotti, 1972) and from early studies on the role of prefrontal lesions on the socioemotional behavior of monkeys (e.g., Myers, 1972). The research featured in this Special Issue is part of a larger body of work (see e.g., Rolls, 1999 for a modern example) that forcefully underscores the importance of prefrontal cortex for emotional and motivational processes.
However, the work represented in this Special Issue has, for the most part, evolved with little connection to the core neuroscience research on the structure and function of the prefrontal cortex. I will argue that this state of affairs must change if this work is to become an accepted part of the influential body of neuroscientific research on the prefrontal cortex. Just what specific role the primate prefrontal cortex (PFC) might be playing in emotion still remains elusive and will be one of the several issues I will address in some detail below. The substantive portions of this commentary will be divided into two parts. The first part will address some of the fundamental conceptual issues that lie at the core of this work, most of which were not addressed in the articles in this Special Issue. I will focus on what the PFC is “doing” in emotion and will draw on other neuroscience literature on PFC from which insights about its role in emotion might be gleaned. In this section, I will also emphasize the fact that the PFC is heterogeneous, both anatomically and functionally and any serious discussion of PFC function must make distinctions among the sub-territories of the PFC. Also to be emphasized is the fact that the PFC is part of a larger overall circuit and that other components of the circuitry are crucial for understanding how the brain implements emotional and motivation processes. It cannot be solely through the prefrontal cortex that the brain implements emotional and motivational processes. One unwitting consequence of the work my laboratory began on prefrontal asymmetries and affect is the view that the prefrontal cortex is the “center” or at least the primary region for all aspects of the emotional and/or motivational processes in question. It is essential that we remind ourselves that the prefrontal cortex is part of a larger and more complex circuit and that other components of this circuitry will undoubtedly be important for many of psychological phenomena of interest to the readers of this Special Issue. A related issue concerns the nature of the measure with which we are dealing. It has been easy for those who study EEG frontal asymmetry to ignore other components of the circuitry because the measure in question here does not reflect many of the other features of the circuit. In particular, scalp-recorded brain electrical signals reflect activity primarily from cortex and without more complex source localization methods which have not been used in any of the articles in this Special Issue, one cannot make inferences about subcortical signals.
Section snippets
Heterogeneity of prefrontal cortex
Many recent reviews have documented the important functional and anatomical divisions within the prefrontal cortex (e.g., Rolls, 1999). For the purposes of the present discussion, it is important to simply call attention to this fact and to indicate that the majority of the neuroscience literature indicates that the prefrontal sector most directly associated with emotion is the sector that is least likely to be reflected in scalp-recorded brain electrical signals—namely, orbital frontal cortex
Evidence of progress
The growing literature on methodological issues in the assessment of EEG asymmetry is leading to important advances that will improve the reliability and validity of these measures. The evidence presented in this Special Issue clearly establishes prefrontal EEG asymmetry measures as reflecting, at least in part, trait-like variations in brain function that appear to predict interesting and important features of affective style. As such, these measures have much to add to our current
Summary and conclusions
This commentary provides some reflections on the current state of affairs in research on EEG frontal asymmetries associated with emotion. The first part addresses a series of conceptual issues and the second part some empirical and methodological issues. Of prime important for the future of EEG asymmetry research is that it make more meaningful contact with the growing corpus of literature on primate prefrontal function. One of the most lamentable characteristics of the current work on frontal
Acknowledgements
I wish to thank the many students, trainees and staff members in my laboratory who have enabled this research program and have been instrumental in it thriving. I particularly wish to thank Jack Nitschke, Alex Shackman, Carien van Reekum, Jim Coan, Tim Salamons and Tom Johnstone for their comments on an earlier draft of this manuscript. I also wish to thank John Allen for his comments on an earlier draft. I also wish to thank the consistent support of NIMH who has funded most of the research
References (73)
- et al.
The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage
Neuropsychologia
(2003) - et al.
Assessing the accuracy of topographic EEG mapping for determining local brain function, Electroencephalography
Electroencephalography and Clinical Neurophysiology
(1998) Anxiety and affective style: role of prefrontal cortex and amygdala
Biological Psychiatry
(2002)Seven sins in the study of emotion: correctives from affective neuroscience
Brain and Cognition
(2003)- et al.
Individual differences in prefrontal activation asymmetry predict natural killer cell activity at rest and in response to challenge
Brain, Behavior, and Immunity
(1999) - et al.
The functional neuroanatomy of emotion and affective style
Trends in Cognitive Science
(1999) Emotional behavior and hemispheric side of lesion
Cortex
(1972)- et al.
Cerebrospinal fluid corticotropin-releasing hormone levels are elevated in monkeys with patterns of brain activity associated with fearful termerament
Biological Psychiatry
(2000) - et al.
EEG-correlated fMRI of human alpha activity
Neuroimage
(2003) - et al.
Experience-dependent asymmetric variation in primate prefrontal morphology
Behavioral and Brain Research
(2002)