Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI

Abstract

We studied error monitoring in a human patient with unique implantation of depth electrodes in both the left dorsal cingulate gyrus and medial temporal lobe prior to surgery. The patient performed a speeded go/nogo task and made a substantial number of commission errors (false alarms). As predicted, intracranial Local Field Potentials (iLFPs) in dorsal anterior cingulate indexed the detection of errors, showing an early differential activity around motor execution for false alarms, relative to correct responses (either hits or correct inhibitions). More surprisingly, we found that the left amygdala also participated to error monitoring (although no emotional stimuli were used), but with a very different neurophysiological profile as compared with the dorsal cingulate cortex. Amygdala iLFPs showed a precise and reproducible temporal unfolding, characterized by an early monophasic response for correct hits around motor execution, which was delayed by ~300 ms for errors (even though actual RTs were almost identical in these two conditions). Moreover, time-frequency analyses demonstrated a reliable and transient coupling in the theta band around motor execution between these two distant regions. Additional fMRI investigation in the same patient confirmed a differential involvement of the dorsal cingulate cortex vs. amygdala in error monitoring during this go/nogo task. Finally, these intracranial results for the left amygdala were replicated in a second patient with intracranial electrodes in the right amygdala. Altogether, these results suggest that the amygdala may register the motivational significance of motor actions on a trial-by-trial basis, while the dorsal anterior cingulate cortex may provide signals concerning failures of cognitive control and behavioral adjustment. More generally, these data shed new light on neural mechanisms underlying self monitoring by showing that even "simple" motor actions recruit not only executive cognitive processes (in dorsal cingulate) but also affective processes (in amygdala).

Early Error Detection Predicted by Reduced Pre-response Control Process: An ERP Topographic Mapping Study

“…Extensive details regarding the stimuli, task parameters and RT calibration procedure used in this experiment can be found in Vocat et al (2008) and Pourtois et al (2010).…”

“…The ERN component is a negative brain potential with a fronto-central scalp distribution (maximum amplitude at FCZ electrode position), peaking early following the onset of erroneous motor responses (typically in a window spanning from 0 until 100 ms after incorrect key presses). The neural generators of the ERN have been consistently localized in the dorsal Anterior Cingulate Cortex across several studies (dACC, see Dehaene, Posner, & Tucker, 1994;Bush, Luu, & Posner, 2000;Debener et al, 2005;van Veen & Carter, 2006;Pizzagalli, Peccoralo, Davidson, & Cohen, 2006;Ridderinkhof, Nieuwenhuis, & Braver, 2007;Vocat, Pourtois, & Vuilleumier, 2008;Pourtois et al, 2010). Time-frequency analyses showed that the ERN was primarily driven by transiently phase-locked theta-band power increase to the subject's motor response (Luu, Tucker, & Makeig, 2004).…”

“…Importantly, I aimed to compare errors to correct hits, when obvious lapses of vigilance did not account for the commission of these errors (see Vocat et al, 2008;Pourtois et al, 2010). More precisely, I predicted that errors would be associated with the marked attenuation of a distinctive anticipatory component, presumably reflecting top-down or proactive attentional control (therefore recruiting regions of the posterior parietal cortex, such as the precuneus; see Li et al, 2007) and hence indirectly contributing to mechanisms of action monitoring (e.g., involved in readying the cognitive system for task performance under high attentional demands, see Barber & Carter, 2005).…”

Functional and anatomical connectivity‐based parcellation of human cingulate cortex

“…The CC is implicated in a diverse array of functions, such as emotion (George et al., 1995; Kross, Davidson, Weber, & Ochsner, 2009; Liotti et al., 2000; Rogers et al., 2004; Rolls, Grabenhorst, & Parris, 2008; Walter et al., 2008, 2009), movement (Beckmann, Johansen‐Berg, & Rushworth, 2009; Paus, 2001; Picard & Strick, 1996, 2001), self‐relevant assessment (Kelley et al., 2002; Vogt, Vogt, & Laureys, 2006), cognition (Luo et al., 2007; Pourtois et al., 2010; Sohn, Albert, Jung, Carter, & Anderson, 2007; Ursu, Clark, Aizenstein, Stenger, & Carter, 2009), memory (Maguire, 2001), visuospatial orientation (Vogt et al., 2006), navigation, imagination, and planning for the future (Vann, Aggleton, & Maguire, 2009). …”

Delayed monitoring of accuracy errors compared to commission errors in ACC

“…Source localization results point to the dorsal anterior cingulate cortex (dACC) as the main generator of both ERN (Dehaene et al, 1994;Yeung et al, 2004;van Veen and Carter, 2006) and FRN (Miltner et al, 1997), and the implication of the dorsal ACC in error detection (and correction) has been confirmed with various neuroimaging techniques, including functional magnetic resonance imaging (fMRI, e.g., Holroyd et al, 2004;Debener et al, 2005), magnetoencephalography (MEG, e.g., Miltner et al, 2003;Keil et al, 2010), and intracranial recordings (Niki and Watanabe, 1979;Brazdil et al, 2002;Halgren et al, 2002;Brazdil et al, 2005;Wang et al, 2005;Emeric et al, 2008;Pourtois et al, 2010).…”