Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function
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
References (23)
The central autonomic network—Functional organization, dysfunction, and perspective
Mayo Clin. Proc.
(1993)AFNI: software for analysis and visualization of functional magnetic resonance neuroimages
Comput. Biomed. Res.
(1996)- et al.
Functional assessment of heart rate variability: physiological basis and practical applications
Int. J. Cardiol.
(2002) - et al.
The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division
Biol. Psychiatry
(1998) - et al.
Linear systems analysis of functional magnetic resonance imaging in human V1
J. Neurosci.
(1996) - et al.
The counting Stroop: an interference task specialized for functional neuroimaging-validation study with functional MRI
Hum. Brain Mapp.
(1998) - et al.
The multi-source interference task: validation study with fMRI in individual subjects
Mol. Psychiatry
(2003) - et al.
Anterior cingulate cortex, error detection, and the online monitoring of performance
Science
(1998) - et al.
Neuroanatomical basis for first- and second-order representations of bodily states
Nat. Neurosci.
(2001) - et al.
Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence
Brain
(2003)
The Feeling of What Happens: Body and Emotion in the Making of Consciousness
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