Volumetric reduction in caudate nucleus following stereotactic lesions of anterior cingulate cortex in humans: a morphometric magnetic resonance imaging study

View More View Less
  • 1 Departments of Psychiatry, Radiology, Neurology, and Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston; and Department of Neurology, McLean Hospital, Belmont, Massachusetts
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object. The goal of this study was to test hypotheses regarding changes in volume in subcortical structures following anterior cingulotomy.

Methods. Morphometric magnetic resonance (MR) imaging methods were used to assess volume reductions in subcortical regions following anterior cingulate lesioning in nine patients. Magnetic resonance imaging data obtained before and 9 ± 6 months following anterior cingulotomy were subjected to segmentation and subcortical parcellation.

Significant volume reductions were predicted and found bilaterally within the caudate nucleus, but not in the amygdala, thalamus, lenticular nuclei, or hippocampus. Subcortical parcellation revealed that the volume reduction in the caudate nucleus was principally referrable to the body, rather than the head. Furthermore, the magnitude of volume reduction in the caudate body was significantly correlated with total lesion volume.

Conclusions. Taken together, these findings implicate significant connectivity between a region of anterior cingulate cortex (ACC) lesioned during cingulotomy and the caudate body. This unique data set complements published findings in nonhuman primates, and advances our knowledge regarding patterns of cortical—subcortical connectivity involving the ACC in humans. Moreover, these findings indicate changes distant from the site of anterior cingulotomy lesions that may play a role in the clinical response to this neurosurgical procedure.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address reprint requests to: Scott L. Rauch, M.D., Department of Psychiatry, Massachusetts General Hospital—East, 9th Floor, Building 149, 13th Street, Charlestown, Massachusetts 02129. email: rauch@psych.mgh.harvard.edu.
  • 1.

    Alexander GE, , Crutcher MD, & DeLong MR: Basal gangliathalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119146, 1990 Alexander GE, Crutcher MD, DeLong MR: Basal gangliathalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146, 1990

    • Search Google Scholar
    • Export Citation
  • 2.

    Baer L, , Rauch SL, & Ballantine HT Jr, et al: Cingulotomy for intractable obsessive-compulsive disorder. Prospective long-term follow-up of 18 patients. Arch Gen Psychiatry 52:384392, 1995 Baer L, Rauch SL, Ballantine HT Jr, et al: Cingulotomy for intractable obsessive-compulsive disorder. Prospective long-term follow-up of 18 patients. Arch Gen Psychiatry 52:384–392, 1995

    • Search Google Scholar
    • Export Citation
  • 3.

    Ballantine HT, & Giriunas IE: Treatment of intractable psychiatric illness and chronic pain by stereotactic cingulotomy, in Schmidek HH, & Sweet WH (eds): Operative Neurosurgical Techniques. New York: Grune & Stratton, 1982, pp 10691075 Ballantine HT, Giriunas IE: Treatment of intractable psychiatric illness and chronic pain by stereotactic cingulotomy, in Schmidek HH, Sweet WH (eds): Operative Neurosurgical Techniques. New York: Grune & Stratton, 1982, pp 1069–1075

    • Search Google Scholar
    • Export Citation
  • 4.

    Brodmann K: Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Barth, 1909 Brodmann K: Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Barth, 1909

    • Search Google Scholar
    • Export Citation
  • 5.

    Caviness VS Jr, , Kennedy DN, & Richelme C, et al: The human brain age 7–11 years: a volumetric analysis based upon magnetic resonance images. Cereb Cortex 6:726736, 1996 Caviness VS Jr, Kennedy DN, Richelme C, et al: The human brain age 7–11 years: a volumetric analysis based upon magnetic resonance images. Cereb Cortex 6:726–736, 1996

    • Search Google Scholar
    • Export Citation
  • 6.

    Caviness VS Jr, , Lange NT, & Makris N, et al: MRI-based brain volumetrics: emergence of a developmental brain science. Brain Dev 21:289295, 1999 Caviness VS Jr, Lange NT, Makris N, et al: MRI-based brain volumetrics: emergence of a developmental brain science. Brain Dev 21:289–295, 1999

    • Search Google Scholar
    • Export Citation
  • 7.

    Cosgrove GR, & Rauch SL: Psychosurgery. Neurosurg Clin North Am 6:167176, 1995 Cosgrove GR, Rauch SL: Psychosurgery. Neurosurg Clin North Am 6:167–176, 1995

    • Search Google Scholar
    • Export Citation
  • 8.

    Dejerine J: Anatomie des Centres Nerveux. Paris: Rueff et Cie, Vol 2, 1895 Dejerine J: Anatomie des Centres Nerveux. Paris: Rueff et Cie, Vol 2, 1895

    • Search Google Scholar
    • Export Citation
  • 9.

    Devinsky O, , Morrell MJ, & Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 118:279306, 1995 Devinsky O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306, 1995

    • Search Google Scholar
    • Export Citation
  • 10.

    Dougherty DD, & Rauch SL: Neuroimaging and neurobiological models of depression. Harvard Rev Psychiatry 5:138159, 1997 Dougherty DD, Rauch SL: Neuroimaging and neurobiological models of depression. Harvard Rev Psychiatry 5:138–159, 1997

    • Search Google Scholar
    • Export Citation
  • 11.

    Drevets WC, , Price JL, & Simpson JR Jr, et al: Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824827, 1997 Drevets WC, Price JL, Simpson JR Jr, et al: Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824–827, 1997

    • Search Google Scholar
    • Export Citation
  • 12.

    Drevets WC, , Videen TO, & Price JL, et al: A functional anatomical study of unipolar depression. J Neurosci 12:36283641, 1992 Drevets WC, Videen TO, Price JL, et al: A functional anatomical study of unipolar depression. J Neurosci 12:3628–3641, 1992

    • Search Google Scholar
    • Export Citation
  • 13.

    Ebert D, , Speck O, & Konig A, et al: 1H magnetic resonance spectroscopy in obsessive compulsive disorder: evidence for neuronal loss in the cingulate gyrus and right striatum. Psychiatr Res Neuroimaging 74:173176, 1997 Ebert D, Speck O, Konig A, et al: 1H magnetic resonance spectroscopy in obsessive compulsive disorder: evidence for neuronal loss in the cingulate gyrus and right striatum. Psychiatr Res Neuroimaging 74:173–176, 1997

    • Search Google Scholar
    • Export Citation
  • 14.

    Filipek PA, , Richelme C, & Kennedy DN, et al: The young adult human brain: an MRI-based morphometric analysis. Cereb Cortex 4:344360, 1994 Filipek PA, Richelme C, Kennedy DN, et al: The young adult human brain: an MRI-based morphometric analysis. Cereb Cortex 4:344–360, 1994

    • Search Google Scholar
    • Export Citation
  • 15.

    Frazier JA, , Giedd JN, & Kaysen D, et al: Childhood-onset schizophrenia: brain MRI rescan after 2 years of clozapine maintenance treatment. Am J Psychiatry 153:564566, 1996 Frazier JA, Giedd JN, Kaysen D, et al: Childhood-onset schizophrenia: brain MRI rescan after 2 years of clozapine maintenance treatment. Am J Psychiatry 153:564–566, 1996

    • Search Google Scholar
    • Export Citation
  • 16.

    Goodman WK, , Price LH, & Rasmussen SA, et al: The Yale-Brown Obsessive Compulsive Scale. Development, use, and reliability. Arch Gen Psychiatry 46:10061011, 1989 Goodman WK, Price LH, Rasmussen SA, et al: The Yale-Brown Obsessive Compulsive Scale. Development, use, and reliability. Arch Gen Psychiatry 46:1006–1011, 1989

    • Search Google Scholar
    • Export Citation
  • 17.

    Kaada BR: Cingulate, posterior orbital, anterior insular and temporal pole cortex, in Magoun HW (ed): Neurophysiology. Baltimore: Waverly Press, 1960, pp 13451372 Kaada BR: Cingulate, posterior orbital, anterior insular and temporal pole cortex, in Magoun HW (ed): Neurophysiology. Baltimore: Waverly Press, 1960, pp 1345–1372

    • Search Google Scholar
    • Export Citation
  • 18.

    Kaada BR, , Pribram KH, & Epstein JA: Respiratory and vascular responses in monkeys from temporal pole, insular, orbital surface and cingulate gyrus: preliminary report. J Neurophysiol 12:348356, 1949 Kaada BR, Pribram KH, Epstein JA: Respiratory and vascular responses in monkeys from temporal pole, insular, orbital surface and cingulate gyrus: preliminary report. J Neurophysiol 12:348–356, 1949

    • Search Google Scholar
    • Export Citation
  • 19.

    Kemp JM, & Powell TPS: The cortico-striate projection in the monkey. Brain 93:525546, 1970 Kemp JM, Powell TPS: The cortico-striate projection in the monkey. Brain 93:525–546, 1970

    • Search Google Scholar
    • Export Citation
  • 20.

    Keshavan MS, , Bagwell WW, & Haas GL, et al: Changes in caudate volume with neuroleptic treatment. Lancet 344:1434, 1994 (Letter) Keshavan MS, Bagwell WW, Haas GL, et al: Changes in caudate volume with neuroleptic treatment. Lancet 344:1434, 1994 (Letter)

    • Search Google Scholar
    • Export Citation
  • 21.

    Kunishio K, & Haber SN: Primate cingulostriatal projection: limbic striatal versus sensorimotor striatal input. J Comp Neurol 350:337356, 1994 Kunishio K, Haber SN: Primate cingulostriatal projection: limbic striatal versus sensorimotor striatal input. J Comp Neurol 350:337–356, 1994

    • Search Google Scholar
    • Export Citation
  • 22.

    Künzle H: Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in macaca fascicularis. Brain Res 88:195209, 1975 Künzle H: Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in macaca fascicularis. Brain Res 88:195–209, 1975

    • Search Google Scholar
    • Export Citation
  • 23.

    Künzle H: Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30:481492, 1977 Künzle H: Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30:481–492, 1977

    • Search Google Scholar
    • Export Citation
  • 24.

    Lippitz BE, , Mindus P, & Meyerson BA, et al: Lesion topography and outcome after thermocapsulotomy or gamma knife capsulotomy for obsessive-compulsive disorder: relevance of the right hemisphere. Neurosurgery 44:452460, 1999 Lippitz BE, Mindus P, Meyerson BA, et al: Lesion topography and outcome after thermocapsulotomy or gamma knife capsulotomy for obsessive-compulsive disorder: relevance of the right hemisphere. Neurosurgery 44:452–460, 1999

    • Search Google Scholar
    • Export Citation
  • 25.

    Makris N, , Meyer JW, & Bates JF, et al: MRI-based topographic parcellation of human cerebral white matter and nuclei. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9:1845, 1999 Makris N, Meyer JW, Bates JF, et al: MRI-based topographic parcellation of human cerebral white matter and nuclei. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9:18–45, 1999

    • Search Google Scholar
    • Export Citation
  • 26.

    Mayberg HS: Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 9:471481, 1997 Mayberg HS: Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 9:471–481, 1997

    • Search Google Scholar
    • Export Citation
  • 27.

    Mayberg HS, , Brannan SK, & Mahurin RK, et al: Cingulate function in depression: a potential predictor of treatment response. Neuroreport 8:10571061, 1997 Mayberg HS, Brannan SK, Mahurin RK, et al: Cingulate function in depression: a potential predictor of treatment response. Neuroreport 8:1057–1061, 1997

    • Search Google Scholar
    • Export Citation
  • 28.

    Mesulam MM: From sensation to cognition. Brain 121:10131052, 1998 Mesulam MM: From sensation to cognition. Brain 121:1013–1052, 1998

    • Search Google Scholar
    • Export Citation
  • 29.

    Mesulam MM: Patterns in behavioral neuroanatomy: association areas, the limbic system, and hemispheric specialization, in Mesulam MM (ed): Principles of Behavioral Neurology. Philadelphia: FA Davis, 1985, pp 170 Mesulam MM: Patterns in behavioral neuroanatomy: association areas, the limbic system, and hemispheric specialization, in Mesulam MM (ed): Principles of Behavioral Neurology. Philadelphia: FA Davis, 1985, pp 1–70

    • Search Google Scholar
    • Export Citation
  • 30.

    Mufson EJ, & Pandya DN: Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol 225:3143, 1984 Mufson EJ, Pandya DN: Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol 225:31–43, 1984

    • Search Google Scholar
    • Export Citation
  • 31.

    Pandya DN, , Van Hoesen GW, & Mesulam MM: Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res 42:319330, 1981 Pandya DN, Van Hoesen GW, Mesulam MM: Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res 42:319–330, 1981

    • Search Google Scholar
    • Export Citation
  • 32.

    Rademacher J, , Galaburda AM, & Kennedy DN, et al: Human cerebral cortex: localization, parcellation, and morphometry with magnetic resonance imaging. J Cogn Neurosci 4:352374, 1992 Rademacher J, Galaburda AM, Kennedy DN, et al: Human cerebral cortex: localization, parcellation, and morphometry with magnetic resonance imaging. J Cogn Neurosci 4:352–374, 1992

    • Search Google Scholar
    • Export Citation
  • 33.

    Rauch SL, , Whalen PJ, & Dougherty DD, et al: Neurobiological models of obsessive compulsive disorders, in Jenike MA, , Baer L, & Minichiello WE (eds): Obsessive-Compulsive Disorders: Practical Management. Boston: Mosby, 1998, pp 222253 Rauch SL, Whalen PJ, Dougherty DD, et al: Neurobiological models of obsessive compulsive disorders, in Jenike MA, Baer L, Minichiello WE (eds): Obsessive-Compulsive Disorders: Practical Management. Boston: Mosby, 1998, pp 222–253

    • Search Google Scholar
    • Export Citation
  • 34.

    Seidman LJ, , Faraone SV, & Goldstein JM, et al: Thalamic and amygdala-hippocampal volume reductions in first-degree relatives of patients with schizophrenia: an MRI-based morphometric analysis. Biol Psychiatry 46:941954, 1999 Seidman LJ, Faraone SV, Goldstein JM, et al: Thalamic and amygdala-hippocampal volume reductions in first-degree relatives of patients with schizophrenia: an MRI-based morphometric analysis. Biol Psychiatry 46:941–954, 1999

    • Search Google Scholar
    • Export Citation
  • 35.

    Spangler WJ, , Cosgrove GR, & Ballantine HT Jr, et al: Magnetic resonance imaging-guided stereotactic cingulotomy for intractable psychiatric disease. Neurosurgery 38:10711078, 1996 Spangler WJ, Cosgrove GR, Ballantine HT Jr, et al: Magnetic resonance imaging-guided stereotactic cingulotomy for intractable psychiatric disease. Neurosurgery 38:1071–1078, 1996

    • Search Google Scholar
    • Export Citation
  • 36.

    Swedo SE, , Schapiro MB, & Grady CL, et al: Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder. Arch Gen Psychiatry 46:518523, 1989 Swedo SE, Schapiro MB, Grady CL, et al: Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder. Arch Gen Psychiatry 46:518–523, 1989

    • Search Google Scholar
    • Export Citation
  • 37.

    Talairach J, & Tournoux P: Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme, 1988 Talairach J, Tournoux P: Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme, 1988

    • Search Google Scholar
    • Export Citation
  • 38.

    Vogt BA, , Finch DM, & Olson CR: Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex 2:435443, 1992 Vogt BA, Finch DM, Olson CR: Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex 2:435–443, 1992

    • Search Google Scholar
    • Export Citation
  • 39.

    Vogt BA, , Nimchinsky EA, & Vogt LJ, et al: Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 359:490506, 1995 Vogt BA, Nimchinsky EA, Vogt LJ, et al: Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 359:490–506, 1995

    • Search Google Scholar
    • Export Citation
  • 40.

    Whalen PJ, , Bush G, & McNally RJ, et al: The Emotional Counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol Psychiatry 44:12191228, 1998 Whalen PJ, Bush G, McNally RJ, et al: The Emotional Counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol Psychiatry 44:1219–1228, 1998

    • Search Google Scholar
    • Export Citation
  • 41.

    Yakovlev PI, & Locke S: Limbic nuclei of thalamus and connections of limbic cortex: corticocortical connections of the anterior cingulate gyrus, the cingulum, and the subcallosal bundle in monkey. Arch Neurol 5:364400, 1961 Yakovlev PI, Locke S: Limbic nuclei of thalamus and connections of limbic cortex: corticocortical connections of the anterior cingulate gyrus, the cingulum, and the subcallosal bundle in monkey. Arch Neurol 5:364–400, 1961

    • Search Google Scholar
    • Export Citation
  • 42.

    Yeterian EH, & Van Hoesen GW: Cortico-striatal projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res 139:4363, 1978 Yeterian EH, Van Hoesen GW: Cortico-striatal projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res 139:43–63, 1978

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 522 86 5
Full Text Views 202 14 0
PDF Downloads 83 11 0
EPUB Downloads 0 0 0