Review
Anatomical insights into the interaction of emotion and cognition in the prefrontal cortex

https://doi.org/10.1016/j.neubiorev.2011.08.005Get rights and content

Abstract

Psychological research increasingly indicates that emotional processes interact with other aspects of cognition. Studies have demonstrated both the ability of emotional stimuli to influence a broad range of cognitive operations, and the ability of humans to use top-down cognitive control mechanisms to regulate emotional responses. Portions of the prefrontal cortex appear to play a significant role in these interactions. However, the manner in which these interactions are implemented remains only partially elucidated. In the present review we describe the anatomical connections between ventral and dorsal prefrontal areas as well as their connections with limbic regions. Only a subset of prefrontal areas are likely to directly influence amygdalar processing, and as such models of prefrontal control of emotions and models of emotional regulation should be constrained to plausible pathways of influence. We also focus on how the specific pattern of feedforward and feedback connections between these regions may dictate the nature of information flow between ventral and dorsal prefrontal areas and the amygdala. These patterns of connections are inconsistent with several commonly expressed assumptions about the nature of communications between emotion and cognition.

Highlights

► Specific prefrontal connections dictate emotion regulation of the amygdala. ► Laminar projection patterns determine flow of information in prefrontal cortex. ► Feedforward and feedback projections challenge prefrontal organization.

Introduction

Accumulating research examines how emotion interacts with other aspects of cognition. Such work has elucidated the ways in which emotionally valenced information can direct or bias attention (Ohman et al., 2001, Most et al., 2005, Mathews and Wells, 1999), and influence decision processes (Knutson et al., 2008). At the same time, a growing literature indicates that cognitive processes such as reappraisal can regulate emotional responses (Jackson et al., 2000, Kim and Hamann, 2007, Ochsner et al., 2002, Ochsner et al., 2004, Ray et al., 2008). Indeed, the interactions between functions that are traditionally defined as strictly emotional or strictly cognitive are substantial enough to call into question the often artificial divide between these domains (see for instance Pessoa, 2008). However, the divide provides conceptual value in that emotional processing has specific characteristics of operation that can be distinguished from other cognitive domains in the same manner in which processes of attention or memory have differing characteristics and are instantiated in different (albeit sometimes partially overlapping) networks of brain regions.

The manner in which emotion and other cognitive domains interact has become increasingly central to models of psychopathology. For example, conceptualizations of anxiety disorders frequently focus on accentuated attentional biases towards threatening stimuli (Bishop, 2007, Cisler and Koster, 2010, Ouimet et al., 2009, Williams et al., 1996). Similarly, failures to apply top down control over emotion are increasingly viewed as central to psychiatric disorders ranging from major depression (Fales et al., 2008, Johnstone et al., 2007, Almeida et al., 2009, Taylor Tavares et al., 2008), to borderline personality disorder (New et al., 2008).

Prefrontal regions figure prominently in neurobiological models of the interface between emotion and other aspects of cognition. However, the anatomical features of different prefrontal regions are often given only cursory attention in considering the validity of such models. To the extent that anatomy is considered, it usually is discussed only in broad terms of whether the area has any direct afferent or efferent connections with limbic regions, such as the amygdala or hypothalamus. However, the details of these connections are essential to understanding these regional interactions. For instance, a model that posits that the dorsolateral prefrontal cortex (DLPFC) directly inhibits amygdalar activity can only be sound if it is demonstrated that the DLPFC sends sufficient direct projections to the amygdala. If such projections are modest or absent, alternative models that rely on intermediary regions will be necessary to explain a posited DLPFC influence on amygdalar responses.

The structural features of different prefrontal regions and the laminar pattern of their connections may also provide substantial insights into the interactions between emotion and cognitive processes mediated by prefrontal cortex (PFC). Specifically, the cytoarchitectural features of different cortical regions dictate the manner in which they process information and interact with other regions. This second level of analysis has generally not entered into discussions of the neural substrates of emotion–cognitive interactions, although it has substantial implications for understanding these processes.

In the present paper, we attempt to outline several features of interregional communication among different PFC areas, and their interactions with the amygdala. We particularly focus on contrasts between orbital and dorsolateral PFC because of long-standing associations of the orbitofrontal cortex (OFC) to emotional processes (Zald and Kim, 1996) and similarly long-standing association of DLPFC to executive aspects of cognition (Fuster, 1989, Stuss and Benson, 1986). We also describe the role of anterior cingulate (ACC)/medial frontal structures in these interactions, as increasing data indicate that these structures provide a critical interface between emotion and other aspects of cognition.

Section snippets

Topography

The PFC is frequently divided into 6 broad regions, dorsolateral, ventrolateral (VLPFC), frontopolar (FP), OFC, ventromedial (VMPFC), and dorsomedial (DMPFC) (see Fig. 1). The exact topographical boundaries of these regions are variably applied by researchers, but the general nomenclature has proven useful as a broad organizing framework for understanding the anatomy and function of the PFC.

Phylogeny and cytoarchitecture

The PFC contains two separable, phylogenetically distinct architectonic trends (Barbas, 1988, Sanides,

Connections

Most existing data on prefrontal connections derives from animal studies. Nevertheless, given the cytoarchitectural homology across primates (Petrides and Mackey, 2006, Ongur et al., 2003), it is generally assumed that the connectivity of these areas is largely conserved across primate species. As such, it is reasonable to use the nonhuman primate literature on connectivity as a basis for evaluating connectivity in humans. We focus on two types of connectivity here: amygdala–PFC connections,

The structural model

The cytoarchitectural features of a cortical region substantially influence how the region interacts with other brain regions. Specifically, the level of granularity and laminar development impact its level of feedforward and feedback projections (Barbas and Rempel-Clower, 1997, Barbas, 2000). Within the model presented by Barbas, feedforward projections are defined structurally as arising from superficial layers and projecting to deep layers of cortex. In sensory systems, early stages of the

Emotion regulation

Emotion regulation has been defined as those processes involved in changing the onset, duration, intensity or content of an emotional response (Gross, 1998, Gross, 2008). Emotion regulation processes range from actions taken long before an emotion arises, such as situation selection, to those processes engaged either just prior to or once an emotion has begun to emerge, such as attention deployment or cognitive reappraisal (Gross, 1998). It is in these latter types of strategies that

Cognitive control of emotional distraction

While much of our analysis has focused on studies of emotion regulation, many similar issues arise when considering the literature on cognitive control. Broadly, cognitive control refers to the high-level executive processes that promote goal relevant processing, while inhibiting goal irrelevant processing. The term is particularly used to apply to tasks requiring the selective attention to incoming goal-relevant sensory information and the inhibition of goal irrelevant sensory information, and

Affective regulation of cognitive areas

Given the structural model outlined in earlier sections, OFC projections to the lateral PFC, including DLPFC can be categorized as predominantly providing feedback. As such, these projections may provide biasing and regulation of more cytoarchitecturally developed regions. Although seemingly opposed to philosophical views that place rationality over emotion, the idea that an area involved in affective processing might provide feedback type biasing over areas involved in other cognitive

Discussion

We believe that the above review illustrates the need to attend to the details of the anatomical connections within the PFC and their relationship to the amygdala when considering emotion–cognition interactions. Failure to do so can lead to models that are difficult to reconcile with anatomy, and are thus likely to prove inaccurate. In contrast, attention to the details of neurocircuitry not only can provide for more plausible models of the interaction between emotional and cognitive processes,

Acknowledgements

This work was supported by grants T32MH018931-21, T32MH018921-20 and 5R01MH074567-04 from the National Institute of Mental Health. We thank Tawny Spinelli for help preparing the manuscript.

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