Elsevier

NeuroImage

Volume 22, Issue 3, July 2004, Pages 1151-1156
NeuroImage

Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function

https://doi.org/10.1016/j.neuroimage.2004.03.005Get rights and content

Abstract

The anterior cingulate cortex (ACC) has diverse functions and several functional subdivisions. This study implemented a counting Stroop task that presented incongruent (INC) and congruent (CON) stimuli at two speeds to probe dorsal (dACC) and ventral (vACC) using functional magnetic resonance imaging (fMRI). Eighteen healthy subjects completed the task twice: once outside the scanner while heart rate variability (HRV) was recorded and once during fMRI. In both sessions, subjects completed two runs. Stimuli were presented every 2.0 s in one run and every 1.5 s in the other. fMRI data analysis revealed two important findings. First, by computing differential activation between INC and CON stimuli, a cluster of activation related to response inhibition was observed in the left dACC. Additionally, by calculating the interaction of speed with stimulus congruency, a cluster of activation was observed in the left vACC. This activation correlated significantly with high-frequency HRV (P < 0.02 for CON and P < 0.003 for INC) and represents the parasympathetic modulatory role of the vACC. This study supports the notion of functional subdivisions within the ACC and links the processes of cognitive interference and parasympathetic modulation with activation in specific subregions of the ACC, a structure that is critical for the interface between cognition and emotion.

Introduction

The anterior cingulate cortex (ACC) is a structure in the medial prefrontal cortex (PFC) with diverse functions. Functional subdivisions have been previously outlined, which distinguish between the cognitive and affective regions within this structure Bush et al., 1998, Vogt et al., 1992, Whalen et al., 1998. In particular, the cognitive (dorsal) division of the ACC is important for mediating processes such as response inhibition (Bush et al., 1998) and error processing (Carter et al., 1998). In comparison, the affective (ventral) subdivision is involved in the processing and integration of emotional information Mayberg, 1997, Simpson et al., 2001.

The neural pathways involved in these processes are closely related to those involved in modulation of the autonomic nervous system (ANS). For example, stimulation of the human rostral cingulate elicits bradycardia and an increase in blood pressure (Pool and Ransohoff, 1949). Cardiovascular responses have also been observed with stimulation of the human orbitofrontal and insular cortices (Oppenheimer et al., 1992), areas that are anatomically and functionally connected to the ACC. Additionally, recent functional magnetic resonance imaging (fMRI) work has demonstrated the importance of the ACC in modulating sympathetic nervous system (SNS) tone (Critchley et al., 2003).

Heart rate variability (HRV) may be viewed as an experimental measure of cardiovascular adaptability. Large variability in heart rate is associated with physical fitness and youth. Conversely, physical and mental illnesses, as well as physical and psychological stressors, are associated with decreased HRV. The sympathetic and parasympathetic subdivisions of the ANS each play a role in regulating heart rate and other homeostatic processes. Postganglionic parasympathetic nervous system (PNS) fibers release acetylcholine (Ach), a neurotransmitter with a rapid onset and course of action. As a result, beat-to-beat (high-frequency) changes in heart rate are mediated by the PNS and reflected in high-frequency HRV. Conversely, SNS neurons release norepinephrine (NE), which is characterized by a slower on/offset. Therefore, SNS influences on heart rate are largely reflected in very low frequency HRV.

The Stroop Word–Color interference task (Stroop, 1935) has been used in psychophysiological studies to probe HRV Delaney and Brodie, 2000, Hoshikawa and Yamamoto, 1997. Additionally, the neural substrates underlying the cognitive processes involved in the Stroop are well characterized and involve the response inhibitory function of the ACC. The current study examined the hypothesis that ANS modulation by the ACC is intimately related to the cognitive processing functions of this structure. To examine this hypothesis, healthy control subjects twice performed a Stroop task: once during functional magnetic resonance imaging (fMRI) and again outside the MRI scanner while HRV was recorded. Because the Stroop task elicits HRV changes in behavioral paradigms Delaney and Brodie, 2000, Hoshikawa and Yamamoto, 1997 and because the ACC has been implicated both in inhibitory function and top-down control of the ANS, we hypothesized that this task would lead to alterations in ANS functioning and brain activation in the ACC. Moreover, we hypothesized that task-induced ANS changes would correlate with task-induced changes in brain activation in the ACC. In the following sections, we will describe the results of this experiment and suggest future research directions that may contribute to the understanding of the link between ACC function and ANS modulation.

Section snippets

Subjects

Eighteen (7 females and 11 males) healthy subjects gave written informed consent and completed the study. The mean age of participants was 39 years (range 27–56), and the average education level of the population was 14.9 years (range 12–18). All subjects completed the structured clinical interview for DSM IV and had no lifetime history of any Axis I DSM IV disorder. The UCSD Human Research Protection Program approved this study.

Task

The current study implemented a counting Stroop task Bush et al.,

Behavioral

Behavioral results are displayed in Table 1. Individual performance was comparable during fMRI and HRV testing sessions. Specifically, during HRV testing, subjects made more errors [F(1, 13) = 131, P < 0.001] and took longer to respond [F(1, 13) = 306, P < 0.001] in the incongruent relative to the congruent trials. Similarly, during fMRI testing, subjects made more errors [F(1, 13) = 86, P < 0.001] and took longer to respond [F(1, 13) = 335, P < 0.001] in the incongruent relative to congruent

Discussion

This study yielded three main results:

  • 1.

    Subjects performed the Stroop task similarly during HRV and fMRI testing.

  • 2.

    Increased task-related ACC activation was observed. As expected, the dACC was activated during the incongruent relative to the congruent condition. Additionally, significant activation of the vACC was observed, which was related to the interaction of task speed by stimulus congruency.

  • 3.

    Within individual subjects, the degree of activation in the vACC, but not the dorsal ACC, correlated

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