Involvement of the anterior cingulate and frontoinsular cortices in rapid processing of salient facial emotional information

Abstract

The anterior cingulate cortex (ACC) and frontoinsular cortex (FI) have been implicated in processing information across a variety of domains, including those related to attention and emotion. However, their role in rapid information processing, for example, as required for timely processing of salient stimuli, is not well understood. Here, we designed an emotional face priming paradigm and employed functional magnetic resonance imaging to elucidate their role in these mechanisms. Target faces with either neutral or fearful emotion were briefly primed by either neutral or fearful faces, or by blank ovals. The pregenual ACC and the FI, together with other regions, such as the amygdala, were preferentially activated in response to fearful face priming, suggesting that these regions are involved in the rapid processing of salient facial emotional information.

Introduction

Most cognitive neuroscience studies on rapid processing of salient emotions such as fear have mainly focused on the role of the amygdala. Many of these studies are based on animal and lesion models using the fear conditioning paradigm (see LeDoux (2000) for a review). However, the idea that the amygdala is the exclusive region that is essential for unconscious, rapid detection of fear has been challenged. For instance, a recent study found that even with bilateral amygdala lesions, patients could rapidly distinguish fearful faces from faces exhibiting other emotions and rapidly categorize faces as being fearful or neutral (Tsuchiya et al., 2009), as opposed to other studies showing the necessity of an intact amygdala for fearful facial affect recognition (Adolphs et al., 1999). It remains unclear how the brain can still rapidly process salient emotional information in the absence of the amygdala. Thus, the roles of other brain structures and pathways involved in fast emotional processing need to be considered.

A cortical network that consists of the anterior cingulate cortex (ACC) and insular cortex is involved in the control of emotional processing (Bush et al., 2000, Carter et al., 1998, Craig, 2009, Critchley et al., 2004). There are anatomical interconnections between the ACC and amygdala (Paus, 2001) and numerous reciprocal connections among the insular cortex and amygdala (Augustine, 1985, Mufson et al., 1981, Phelps et al., 2001), ACC, other limbic structures, and various regions of the frontal, temporal, and parietal lobes (Augustine, 1985). A role of the insular cortex as a relay to limbic areas has previously been hypothesized (Geschwind, 1965), and is supported by functional imaging studies of empathy (Carr et al., 2003, Gu and Han, 2007, Gu et al., 2010, Jackson et al., 2005, Singer et al., 2004) and lesion studies on the affective component of pain perception and threat-related responses (Berthier et al., 1988). These findings suggest that the ACC and insular cortex play a significant role in emotional response and regulation. However, an overlapping circuitry involving the ACC and insula has also been implicated across a wide variety of cognitive tasks (Nee et al., 2007). Therefore, the role of these structures may relate more to rapid processing of information in general, rather than specifically to emotional processing.

One such piece of evidence for the anatomical specialization of these regions is the presence of large, bipolar, spindle shaped neurons referred to as von Economo neurons (VENs). VENs have previously been described in humans and great apes (Nimchinsky et al., 1999) and have since been described in cetaceans (Butti et al., 2009, Hof and Van der Gucht, 2007) and in elephants (Hakeem et al., 2009). VENs are most abundant in humans and are primarily found in clusters in layer Vb in the ACC with highest densities in areas 24b and 24a, and are also found in a cytoarchitectonically distinct region located in the junction of the posterior orbitofrontal cortex and the anterior insular cortex known as the frontoinsular cortex (FI) (Allman et al., 2005, Nimchinsky et al., 1999, Nimchinsky et al., 1995, Von Economo and Koskinas, 1925). VENs are projection neurons approximately 4.6 times the size of neighboring pyramidal neurons and are morphologically well-suited for rapid, long distance integration of information (Allman et al., 2005). The distribution of VENs is restricted to highly specific cortical regions (ACC and FI), which are associated with functions including executive control of attention (Botvinick et al., 2001, Fan et al., 2003, Fan et al., 2005, MacDonald et al., 2000), emotional regulation (Bush et al., 2000), and both empathy and experienced pain (Singer et al., 2004). Therefore, the ACC and FI may play a role in our ability to rapidly integrate information amongst spatially distinct functional regions and make quick and intuitive judgments regarding uncertain and rapidly changing social contexts (Allman et al., 2005).

Merging perspectives from studies of the role of the ACC and FI in emotional processing with those from other cognitive domains may provide unique insight into the function of these structures. We hypothesized that the ACC and FI are involved in rapid processing of salient facial emotional information such as fear. For the purposes of our current inquiry, we designed an emotional face priming paradigm in which participants were asked to make a decision regarding the emotional valence of a target face (neutral or fearful) that was primed briefly either by a face expressing neutral or fearful affect, or by a non-face object. The prime was designed to be orthogonal to the target response, therefore did not have predictive value and could be ignored. If the prime impacts the target response, this indicates a positive or negative priming effect and implies that the prime is processed rapidly. Comparison between the non-face and face primes allows us to examine the role of these regions in rapid processing of faces, and comparison between fearful and neutral face primes is intended to examine regions involved in rapid processing of salient emotional expression. We expected fearful face primes to activate the ACC and the FI in the rapid processing of salient emotion primes.