Background
In view of conflicting neuroimaging results regarding autonomic-specific activity
within the anterior cingulate cortex (ACC), we investigated autonomic responses to
direct brain stimulation during stereotactic limbic surgery.
Methods
Skin conductance activity and accelerative heart rate responses to multi-voltage stimulation
of the ACC (n = 7) and paralimbic subcaudate (n = 5) regions were recorded during bilateral anterior cingulotomy and bilateral subcaudate
tractotomy (in patients that had previously received an adequate lesion in the ACC),
respectively.
Results
Stimulations in both groups were accompanied by increased autonomic arousal. Skin
conductance activity was significantly increased during ACC stimulations compared
with paralimbic targets at 2 V (2.34 ± .68 [score in microSiemens ± SE] vs. .34 ±
.09, p = .013) and 3 V (3.52 ± .86 vs. 1.12 ± .37, p = .036), exhibiting a strong “voltage-response” relationship between stimulus magnitude
and response amplitude (difference from 1 to 3 V = 1.15 ± .90 vs. 3.52 ± .86, p = .041). Heart rate response was less indicative of between-group differences.
Conclusions
This is the first study of its kind aiming at seeking novel insights into the mechanisms
responsible for central autonomic modulation. It supports a concept that interregional
interactions account for the coordination of autonomic arousal.
Key Words
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References
- Cognitive and emotional influences in anterior cingulate cortex.Trends Cogn Sci. 2000; 4: 215-222
- Pain and emotion interactions in the subregions of the cingulate gyrus.Nat Rev Neurosci. 2005; 6: 533-544
- Contributions of anterior cingulate cortex to behaviour.Brain. 1995; 118: 279-306
- Functional neuroanatomy of the prefrontal cortex: Autonomic interactions.Prog Brain Res. 2000; 126: 49-62
- Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expressions.BMC Neurosci. 2003; 4: 25
- Free will versus survival: Brain systems that underlie intrinsic constraints on behavior.J Comp Neurol. 2005; 493: 132-139
- Prefrontal-subcortical pathways mediating successful emotion regulation.Neuron. 2008; 59: 1037-1050
- Neural mechanisms of autonomic, affective, and cognitive integration.J Comp Neurol. 2005; 493: 154-166
- Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease.Proc Natl Acad Sci U S A. 1998; 95: 6454-6459
- Neural activity relating to generation and representation of Galvanic skin conductance responses: A functional magnetic resonance imaging study.J Neurosci. 2000; 20: 3033-3040
- The neural correlates of orienting: An integration of fMRI and skin conductance orienting.Neuroreport. 2000; 11: 3011-3015
- Task-independent functional brain activity correlation with skin conductance changes: An fMRI study.Neuroimage. 2002; 17: 1797-1806
- Anterior cingulate activity during error and autonomic response.Neuroimage. 2005; 27: 885-895
- Activity in the ventromedial prefrontal cortex covaries with sympathetic skin conductance level: A physiological account of a “Default Mode” of brain function.Neuroimage. 2004; 22: 243-251
- Autonomic and prefrontal cortex responses to autobiographical recall of emotions.Cogn Affect Behav Neurosci. 2007; 7: 243-250
- Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function.Neuroimage. 2004; 22: 1151-1156
- Functional neuroanatomical correlates of electrodermal activity: A positron emission tomographic study.Psychophysiology. 1998; 35: 179-185
- Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans.J Physiol. 2000; 523: 259-270
- Neuroanatomical basis for first- and second-order representations of bodily states.Nat Neurosci. 2001; 4: 207-212
- Neural activity in the human brain relating to uncertainty and arousal during anticipation.Neuron. 2001; 29: 537-545
- Brain activity during biofeedback relaxation: A functional neuroimaging investigation.Brain. 2001; 124: 1003-1012
- Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence.Brain. 2003; 126: 2139-2152
- Disorders of the autonomic nervous system.in: Bradley W.G. Daroff R.B. Fenichel G.M. Neurology in Clinical Practice. Butterworths-Heinemann, Woburn, Massachusetts2000: 2131-2165
- The functional significance of the rostral cingular cortex as revealed by its responses to electrical stimulation.J Neurophysiol. 1945; 8: 241-255
- Autonomic and somatic reactions induced by stimulation of the cingular Gyrus in dogs.J Neurophysiol. 1947; 10: 371-379
- Respiratory and vascular responses in monkeys from temporal pole insula, orbital surface and cingulate gyrus; a preliminary report.J Neurophysiol. 1949; 12: 347-356
- The cingular gyrus: Area 24.J Neurophysiol. 1948; 11: 13-23
- Autonomic effects on stimulating rostral portion of cingulate gyri in man.J Neurophysiol. 1949; 12: 358-392
- Direct electrical stimulation of specific human brain structures and bilateral electrodermal activity.Int J Psychophysiol. 1996; 22: 1-8
- Towards a network theory of cognition.Neural Netw. 2000; 13: 861-870
- Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function.Psychophysiology. 2007; 44: 343-351
- Prospective long-term follow-up of 44 patients who received cingulotomy for treatment-refractory obsessive-compulsive disorder.Am J Psychiatry. 2002; 159: 269-275
- Prospective assessment of stereotactic ablative surgery for intractable major depression.Biol Psychiatry. 2008; 64: 449-454
- Physiologic responses to loud tones in Vietnam veterans with posttraumatic stress disorder.J Abnorm Psychol. 1995; 104: 75-82
- Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI.Neuroimage. 2002; 16: 331-348
- Volitional control of autonomic arousal: A functional magnetic resonance study.Neuroimage. 2002; 16: 909-919
- Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: Implication for interactions between emotion and cognition.Cogn Emotion. 1998; 12: 353-385
- Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting Stroop.Biol Psychiatry. 1999; 45: 1542-1552
- The anatomy of melancholia-focal abnormalities of cerebral blood flow in major depression.Psychol Med. 1992; 22: 607-615
- Limbic-cortical dysregulation: A proposed model of depression.J Neuropsychiatr Clin Neurosci. 1997; 9: 471-481
- Neural correlates of levels of emotional awareness. evidence of an interaction between emotion and attention in the anterior cingulate cortex.J Cogn Neurosci. 1998; 10: 525-535
- Volitional facilitation of difficult intentions: Joint activation of intention, memory and positive affect removes Stroop interference.J Exp Psychol Gen. 1999; 128: 382-399
- A neuropsychological theory of positive affect and its influence on cognition.Psychol Rev. 1999; 106: 529-550
- Neuroanatomical correlates of electrodermal skin conductance responses.Psychophysiology. 1994; 31: 427-438
- Personality changes after operations on the cingulate gyrus in Man.J Neurol Neurosurg Psychiatry. 1953; 16: 186-193
- Safety and efficacy of cingulotomy for pain and psychiatric disorder.in: Hitchcock E.R. Ballantine H.T. Yerson B.A. Modern Concepts in Psychiatric Surgery. Elsevier/North-Holland, Biomedical Publishing, New York1979: 253-272
- Review of long-term results of stereotactic psychosurgery.Neurol Med Chir. 2002; 42: 365-371
- Long-term outcome of neurosurgery for the treatment of resistant depression.J Neuropsychiatr Clin Neurosci. 2005; 17: 478-485
- The Cognitive Control Network: Integrated cortical regions with dissociable functions.Neuroimage. 2007; 37: 343-360
Article info
Publication history
Published online: June 22, 2009
Accepted:
May 8,
2009
Received in revised form:
April 13,
2009
Received:
January 27,
2009
Identification
Copyright
© 2009 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.