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Axon bundle spacing in the anterior cingulate cortex of the human brain
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Journal of Clinical Neuroscience 15 (2008) 1389–1392 www.elsevier.com/locate/jocn
Short Communication
Axon bundle spacing in the anterior cingulate cortex of the human brain Enrica Di Rosa a, Timothy J. Crow b, Steven A. Chance b,c,* a
Dipartimento di Neuroscienze, Scienze Psichiatriche e Anestesiologiche, Universita´ di Messina, Italy b SANE-POWIC, Warneford Hospital, Oxford, Headington, UK c Neuropathology, West Wing, John Radcliffe Hospital, Oxford, Headington, OX3 9DU, UK Received 20 December 2007; accepted 21 January 2008
Abstract The anterior cingulate cortex (ACC) is implicated in neuropsychiatric disorders. Post-mortem axon bundle data will be important to complement novel MRI methods for analysing cortical diffusion data. [Jespersen SN, Kroenke CD, Ostergaard L, et al. Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage. 2007;34:1473–86] Therefore we aimed to assess perimeter, area, density and spacing of axon bundles in BA24 not previously measured in the human ACC using image analysis of 10 lm-thick tangential sections of layer IV in 4 normal patients. Axon bundle mean perimeter was 53.8 lm, mean area was 197.1 lm2, mean density was 226.3/mm2, and mean spacing was 73.8 lm. Thus, axon bundles were widely spaced relative to cell body minicolumns and other prelimbic areas. A review of the literature suggests that there is hierarchical regional variation of bundle and column spacing. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Anterior cingulate cortex; Brain development; Minicolumn; Neuroplasticity; White matter
1. Introduction In the human brain, the anterior cingulate cortex (ACC) has a role in reward anticipation, decision-making, empathy, and emotion. Intracortical and intercortical connections are organised here with a minicolumnar pattern formed during embryogenesis.2 Neuroimaging and postmortem studies have implicated axon bundles, myelination and minicolumnar abnormalities in some psychiatric disorders.3–5 ACC minicolumn spacing based on cell body distribution has been measured in the rhesus monkey6 and humans.7 Gabbott and Bacon reported cell minicolumn and dendrite bundle densities in prelimbic areas 25 and 32 in the human brain.8 However, the axonal system has not been examined in area 24, which constitutes the bulk of the ACC. This brief survey measured perimeter, area and density of axon bundles in Brodman area (BA) 24 of the ACC, in layer 4, between 800 lm and 900 lm depth, based on *
Corresponding author. Tel.: +44 1 8652 34934; fax: +44 1 8654 55922. E-mail address: [email protected] (S.A. Chance).
0967-5868/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2008.01.018
cytoarchitectural criteria. Axons form clear clusters here as they descend from supragranular cell minicolumns in layer 3.9,10 We compare Gabbott’s minicolumn and dendritic bundle measurements of BA25 and BA32 with the broader literature on minicolumn organisation, particularly in humans. 2. Materials and methods 2.1. Patients and tissue samples We used the brain tissue from BA24 (ACC) of four normal patients. All material had been in fixative for longer than one year, enough to stabilize shrinkage, estimated at 24% for these samples.11 Tissue storage and processing procedures are described elsewhere.12 Neuropathological assessment by consultants (MM Esiri and B McDonald, Oxford) excluded cases with significant pathology. One 5 mm3 block was sampled from each hemisphere at a systematically randomised point between the anterior boundary of the corpus callosum and the anterior commissure, and embedded in paraffin wax. Tangential 10 lm sec-
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E.D. Rosa et al. / Journal of Clinical Neuroscience 15 (2008) 1389–1392
tions were cut by rotary microtome and stained using Palmgren’s silver.13–15 One section per hemisphere was used for measurement. 2.2. Image analysis Patches of 150,000 lm2 were imaged using commercial software (Zeiss KS300, Carl Zeiss Vision GmbH, Mu¨nchen, Germany/Imaging Associates Ltd, Thame, Oxfordshire, UK) through a light microscope (60 lens). Single bundles of vertical fibres were visually identified and measured semi-automatically (Fig. 1). Bundle number and centre-to-centre distance in each image were recorded based on a hexagonal distribution.9,16 A Pearson’s correlation coefficient showed optimal intra-observer reliability (p = 0.011). 3. Results We have presented raw data uncorrected for shrinkage as this may introduce an additional component of measurement error. The mean perimeters of the axon bundles were: left hemisphere, 52.4 lm (SD 2.3 lm); right hemisphere, 55.1 lm (SD 4.6 lm). The mean areas of axon bundles were: left hemisphere, 189.9 lm2 (SD 15.5 lm2); right hemisphere, 204.2 lm2 (SD 29.9 lm2). The mean cluster densities per mm2 were: left hemisphere, 234.5 (SD 68.5); right hemisphere, 218 (SD 38.9). The mean spacing between column bundles was calculated as: left hemisphere, 70.2 lm (SD 8.5 lm); right hemisphere, 77.4 lm (SD 6.5 lm). No significant interhemispheric difference was found regarding minicolumn perimeter, area, density or spacing. However, the statistics have limited power because of the small number of cases (Table 1). 4. Discussion Gabbott reported a distance of 52–59 lm between apical dendrite bundles in Brodmann’s areas 25, 32 and 32’ of the human brain.9 Axon bundle spacing in other areas is reported at the low end of the range: 30–35 lm17,18 and cell body minicolumn spacing in area 24 at 40 lm.7 Methodological differences might explain the wider distribution of axon bundles found here. However, although their overall
Fig. 1. A 10 lm tangential section of layer IV of the anterior cingulate cortex (ACC) stained with Palmgren silver solution. Axon bundles are outlined in black (60).
spatial regularity is very similar, a precise spatial coincidence between cell body minicolumns, dendrite and axonal bundles is uncertain. In the cingulate cortex the diameter of macrocolumnar neuron patches has been reported at 300–320 lm.19 The present data from this study combined with the data from Table 2 suggest that there are about 30 axon bundles per macrocolumn in the limbic cingulate cortex. Despite the methodological variation between studies, there is evidence of a hierarchical variation of columnar organisation (Table 2). This places the limbic cortex (posterior and anterior cingulate) at the lower end of the scale: primary sensory cortex, 52 lm; limbic cortex, 53 lm; unimodal sensory association cortex, 59 lm; polymodal asso-
Table 1 Axon bundle perimeter and area, density, and centre-to-centre axon bundle spacing Case no.
Age
Sex
L perim. (lm)
R perim. (lm)
L area (lm2)
R area (lm2)
L dens. (N/mm2)
R dens. (N/mm2)
L spacing (lm)
R spacing (lm)
1092 1186 1388 14
88 80 75 66
F F M M
53.4 54.0 48.9 53.3
61.6 51.9 54.7 52.1
196.8 202.3 167.4 193.0
244.6 187.8 207.8 176.5
188 221 194 335
188 248 255 181
78.4 72.2 77.2 59.8
78.4 68.2 67.2 79.8
(SD (SD (SD (SD
9.5) 10.3) 6.8) 6.9)
(SD (SD (SD (SD
10.6) 8.6) 7.7) 6.2)
(SD (SD (SD (SD
77.6) 76.0) 45.7) 44.8)
(SD (SD (SD (SD
70.7) 71.7) 59.7) 36.2)
L = left hemisphere, R = right hemisphere, perim. = perimeter, dens. = density, SD = standard deviation. Subjects are identified by a randomly assigned code, age and sex.
E.D. Rosa et al. / Journal of Clinical Neuroscience 15 (2008) 1389–1392
1391
Table 2 Studies of the distribution of minicolumn elements by cortical region. Mean spacing is derived from the periodicity of all columnar elements reported for a region, including cell bodies, axon bundles and dendrites. Data are from published findings on adult humans (excluding Down’s syndrome) Brodmann area
Spacing (lm)
No. of studies
Mean spacing (lm)
Region name
Hierarchical role
Studies
38 21 20 41 42
30 30–86 23–30 46–75 45–83
1 2 2 2 2
30 58 26.5 60.5 64
Inferior temporal cortex
Del Rio & DeFelipe 199717 Del Rio & DeFelipe 199717; Chance et al. 200620 Del Rio & DeFelipe 199717; Di Rosa et al. 200621 Seldon 198126; Chance et al. 200620
22
34–83
6
60
25
50–60
1
55
General sensory association cortex Auditory projection cortex Auditory association cortex Limbic and Prelimbic Cortex
32,32’
50–60
1
55
23 24 31 7
40 40–73* 40 40–80
1 2 1 2
40 56.5 40 60
19
35–40
2
37.5
Posterior parietal lobe
17
16–80
3
40
Occipital lobe
9
70
1
70
Premotor cortex
4
80
1
80
Precentral gyrus
40
80
1
80
Supramarginal lobe
*
Middle 1/3 of Superior Temporal Cortex Superior temporal gyrus Sub genual cingulate Dorsal pregenual anterior cingulate Posterior cingulate Anterior cingulate Precuneus Superior parietal lobule
Buldyrev et al. 200022; Buxhoeveden et al. 200123; Buxhoeveden et al 199624; Casanova et al. 200225; Chance et al. 200620; Seldon 198126 Gabbott et al. 20039 Gabbott et al. 20039
Parietal cortex General sensory association cortex Visual association cortex Visual projection cortex Motor association cortex (dlpfc) Primary motor cortex Somatosensory association cortex
Schlaug et al. 19957 Schlaug et al. 19957; DiRosa et al.* Schlaug et al. 19957 VonBonin & Mehler 197127; Schlaug et al. 19957
Kenan-Vaknin et al. 199218; Schlaug et al 19957
Buxhoeveden et al. 19968; VonBonin & Mehler 197127; Morgane et al. 198828 Casanova et al. 200710
VonBonin & Mehler 197127 VonBonin & Mehler 197128
=current study.
ciation cortex, 56 lm; parieto-occipito-temporal junction (Wernicke’s area), 68 lm. These data suggest a regional hierarchy of organisation of axon bundles and minicolumns in the human brain. Notwithstanding variation in the degree of columnarity20, it is found increasingly that the distribution of minicolumn spacing is 20–90 lm. In measuring cell body arrangement, as well as axon and dendrite bundles, the mean spacing across many studies converges on the range 50–60 lm. References 1. Jespersen SN, Kroenke CD, Ostergaard L, et al. Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage 2007;34:1473–86. 2. Jones EG. Minicolumns in the cerebral cortex. Proc Natl Acad Sci USA 2000;97:5019–21. 3. Szeszko PR, Ardekani BA, Ashtari M, et al. White matter abnormalities in obsessive-compulsive disorder: a diffusion tensor imaging study. Arch Gen Psychiatry 2005;62:782–90. 4. Bae JN, MacFall JR, Krishnan KR, et al. Dorsolateral prefrontal cortex and anterior cingulate cortex white matter alterations in latelife depression. Biol Psychiatry 2006;60:1356–63.
5. McCullumsmith D, Gupta M, Beneyto E, et al. Expression of transcripts for myelination-related genes in the anterior cingulate cortex in schizophrenia? Schizophrenia Research 2007;90:15–27 R. 6. Arikuni T, Sakai M, Kubota K. Columnar aggregation of prefrontal and anterior cingulate cortical cells projecting to the thalamic mediodorsal nucleus in the monkey. J Comp Neurol 1983;220:116–25. 7. Schlaug G, Schleicher A, Zilles K. Quantitative analysis of the columnar arrangement of neurons in the human cingulate cortex. J Comp Neurol 1995;351:441–52. 8. Gabbott PL, Bacon SJ. The organization of dendritic bundles in the prelimbic cortex (area 32) of the rat. Brain Res 1996;730:75–86. 9. Gabbott PL. Radial organization of neurons and dendrites in human cortical areas 25, 32, and 32’D. P Brain Research 2003;992:298–304. 10. Casanova MF, Switala AE, Trippe J. A comparison study of the vertical bias of pyramidal cells in the hippocampus and neocortex. Dev Neurosci 2007;29:193–200. 11. Quester R, Schroder R. The shrinkage of the human brain stem during formalin fixation and embedding in paraffin. J Neurosci Methods 1997;75:81–9. 12. McDonald B, Highley JR, Walker MA, et al. Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: A postmortem study. Am J Psychiatry 2000;157:40–7. 13. Chance SA, Highley JR, Esiri MM, et al. Fiber content of the fornix in schizophrenia: lack of evidence for a primary limbic encephalopathy. Am J Psych 1999;156:1720–4.
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E.D. Rosa et al. / Journal of Clinical Neuroscience 15 (2008) 1389–1392
14. Bancroft J, Stevens A, Theory and practice of histological techniques, ISBN: 0-443-04760-X, Churchill Livingstone. 1996. 15. Murray M, Wang SD, Goldberger ME, et al. Modification of astrocytes in the spinal cord following dorsal root or peripheral nerve lesions. Exp Neurol 1990;110:248–57. 16. Favorov OV, Kelly DG. Minicolumnar organization within somatosensory cortical segregates: II. Emergent functional properties. Cereb Cortex 1994;4:428–42. 17. Del Rio MR, DeFelipe J. Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J Chem Neuroanat 1997;13:243–51. 18. Kenan-Vaknin G, Ouaknine GE, Razon N, et al. Organization of layers II–III connections in human visual cortex revealed by in vitro injections of biocytin. Brain Res 1992;594:339–42. 19. Benes FM, Bird ED. An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Arch Gen Psychiatry 1987;44:608–16. 20. Chance SA, Casanova MF, Switala AE, et al. Minicolumn thinning in temporal lobe association cortex but not primary auditory cortex in normal human ageing. Acta Neuropathol (Berl) 2006;111:459–64.
21. Di Rosa E, Chance SA, Walker MA, et al. Reduced neuron density in fusiform cortex in schizophrenia. Schiz Res 2006;81 Supplement: 209–10. 22. Buldyrev SV, Cruz L, Gomez-Tortosa E, et al. Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias. Proc Natl Acad Sci USA 2000;97:5039–43. 23. Buxhoeveden D, Switala E, Roy M, et al. Morphological differences between minicolumns in human and non-human primate cortex. Am J Phys Anthropol 2001;115:361–71. 24. Buxhoeveden D, Lefkowitz W, Loats P, et al. The linear organization of cell columns in human and nonhuman anthropoid Tpt cortex. Anat Embryol (Berl) 1996;194:23–36. 25. Casanova MF, Buxhoeveden DP, Cohen M, et al. Minicolumnar pathology in dyslexia. Ann Neurol 2002;52:108–10. 26. Seldon HL. Structure of human auditory cortex. I. Cytoarchitectonics and dendritic distributions. Brain Res 1981;229:277–94. 27. Von Bonin G, Mehler WR. On columnar arrangement of nerve cells in cerebral cortex. Brain Res 1971;27:1–9. 28. Morgane PJ, Glezer II, Jacobs MS. Visual cortex of the dolphin: an image analysis study. J Comp Neurol 1988;273:3–25.
Journal of Clinical Neuroscience 15 (2008) 1389–1392 www.elsevier.com/locate/jocn
Short Communication
Axon bundle spacing in the anterior cingulate cortex of the human brain Enrica Di Rosa a, Timothy J. Crow b, Steven A. Chance b,c,* a
Dipartimento di Neuroscienze, Scienze Psichiatriche e Anestesiologiche, Universita´ di Messina, Italy b SANE-POWIC, Warneford Hospital, Oxford, Headington, UK c Neuropathology, West Wing, John Radcliffe Hospital, Oxford, Headington, OX3 9DU, UK Received 20 December 2007; accepted 21 January 2008
Abstract The anterior cingulate cortex (ACC) is implicated in neuropsychiatric disorders. Post-mortem axon bundle data will be important to complement novel MRI methods for analysing cortical diffusion data. [Jespersen SN, Kroenke CD, Ostergaard L, et al. Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage. 2007;34:1473–86] Therefore we aimed to assess perimeter, area, density and spacing of axon bundles in BA24 not previously measured in the human ACC using image analysis of 10 lm-thick tangential sections of layer IV in 4 normal patients. Axon bundle mean perimeter was 53.8 lm, mean area was 197.1 lm2, mean density was 226.3/mm2, and mean spacing was 73.8 lm. Thus, axon bundles were widely spaced relative to cell body minicolumns and other prelimbic areas. A review of the literature suggests that there is hierarchical regional variation of bundle and column spacing. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Anterior cingulate cortex; Brain development; Minicolumn; Neuroplasticity; White matter
1. Introduction In the human brain, the anterior cingulate cortex (ACC) has a role in reward anticipation, decision-making, empathy, and emotion. Intracortical and intercortical connections are organised here with a minicolumnar pattern formed during embryogenesis.2 Neuroimaging and postmortem studies have implicated axon bundles, myelination and minicolumnar abnormalities in some psychiatric disorders.3–5 ACC minicolumn spacing based on cell body distribution has been measured in the rhesus monkey6 and humans.7 Gabbott and Bacon reported cell minicolumn and dendrite bundle densities in prelimbic areas 25 and 32 in the human brain.8 However, the axonal system has not been examined in area 24, which constitutes the bulk of the ACC. This brief survey measured perimeter, area and density of axon bundles in Brodman area (BA) 24 of the ACC, in layer 4, between 800 lm and 900 lm depth, based on *
Corresponding author. Tel.: +44 1 8652 34934; fax: +44 1 8654 55922. E-mail address: [email protected] (S.A. Chance).
0967-5868/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2008.01.018
cytoarchitectural criteria. Axons form clear clusters here as they descend from supragranular cell minicolumns in layer 3.9,10 We compare Gabbott’s minicolumn and dendritic bundle measurements of BA25 and BA32 with the broader literature on minicolumn organisation, particularly in humans. 2. Materials and methods 2.1. Patients and tissue samples We used the brain tissue from BA24 (ACC) of four normal patients. All material had been in fixative for longer than one year, enough to stabilize shrinkage, estimated at 24% for these samples.11 Tissue storage and processing procedures are described elsewhere.12 Neuropathological assessment by consultants (MM Esiri and B McDonald, Oxford) excluded cases with significant pathology. One 5 mm3 block was sampled from each hemisphere at a systematically randomised point between the anterior boundary of the corpus callosum and the anterior commissure, and embedded in paraffin wax. Tangential 10 lm sec-
1390
E.D. Rosa et al. / Journal of Clinical Neuroscience 15 (2008) 1389–1392
tions were cut by rotary microtome and stained using Palmgren’s silver.13–15 One section per hemisphere was used for measurement. 2.2. Image analysis Patches of 150,000 lm2 were imaged using commercial software (Zeiss KS300, Carl Zeiss Vision GmbH, Mu¨nchen, Germany/Imaging Associates Ltd, Thame, Oxfordshire, UK) through a light microscope (60 lens). Single bundles of vertical fibres were visually identified and measured semi-automatically (Fig. 1). Bundle number and centre-to-centre distance in each image were recorded based on a hexagonal distribution.9,16 A Pearson’s correlation coefficient showed optimal intra-observer reliability (p = 0.011). 3. Results We have presented raw data uncorrected for shrinkage as this may introduce an additional component of measurement error. The mean perimeters of the axon bundles were: left hemisphere, 52.4 lm (SD 2.3 lm); right hemisphere, 55.1 lm (SD 4.6 lm). The mean areas of axon bundles were: left hemisphere, 189.9 lm2 (SD 15.5 lm2); right hemisphere, 204.2 lm2 (SD 29.9 lm2). The mean cluster densities per mm2 were: left hemisphere, 234.5 (SD 68.5); right hemisphere, 218 (SD 38.9). The mean spacing between column bundles was calculated as: left hemisphere, 70.2 lm (SD 8.5 lm); right hemisphere, 77.4 lm (SD 6.5 lm). No significant interhemispheric difference was found regarding minicolumn perimeter, area, density or spacing. However, the statistics have limited power because of the small number of cases (Table 1). 4. Discussion Gabbott reported a distance of 52–59 lm between apical dendrite bundles in Brodmann’s areas 25, 32 and 32’ of the human brain.9 Axon bundle spacing in other areas is reported at the low end of the range: 30–35 lm17,18 and cell body minicolumn spacing in area 24 at 40 lm.7 Methodological differences might explain the wider distribution of axon bundles found here. However, although their overall
Fig. 1. A 10 lm tangential section of layer IV of the anterior cingulate cortex (ACC) stained with Palmgren silver solution. Axon bundles are outlined in black (60).
spatial regularity is very similar, a precise spatial coincidence between cell body minicolumns, dendrite and axonal bundles is uncertain. In the cingulate cortex the diameter of macrocolumnar neuron patches has been reported at 300–320 lm.19 The present data from this study combined with the data from Table 2 suggest that there are about 30 axon bundles per macrocolumn in the limbic cingulate cortex. Despite the methodological variation between studies, there is evidence of a hierarchical variation of columnar organisation (Table 2). This places the limbic cortex (posterior and anterior cingulate) at the lower end of the scale: primary sensory cortex, 52 lm; limbic cortex, 53 lm; unimodal sensory association cortex, 59 lm; polymodal asso-
Table 1 Axon bundle perimeter and area, density, and centre-to-centre axon bundle spacing Case no.
Age
Sex
L perim. (lm)
R perim. (lm)
L area (lm2)
R area (lm2)
L dens. (N/mm2)
R dens. (N/mm2)
L spacing (lm)
R spacing (lm)
1092 1186 1388 14
88 80 75 66
F F M M
53.4 54.0 48.9 53.3
61.6 51.9 54.7 52.1
196.8 202.3 167.4 193.0
244.6 187.8 207.8 176.5
188 221 194 335
188 248 255 181
78.4 72.2 77.2 59.8
78.4 68.2 67.2 79.8
(SD (SD (SD (SD
9.5) 10.3) 6.8) 6.9)
(SD (SD (SD (SD
10.6) 8.6) 7.7) 6.2)
(SD (SD (SD (SD
77.6) 76.0) 45.7) 44.8)
(SD (SD (SD (SD
70.7) 71.7) 59.7) 36.2)
L = left hemisphere, R = right hemisphere, perim. = perimeter, dens. = density, SD = standard deviation. Subjects are identified by a randomly assigned code, age and sex.
E.D. Rosa et al. / Journal of Clinical Neuroscience 15 (2008) 1389–1392
1391
Table 2 Studies of the distribution of minicolumn elements by cortical region. Mean spacing is derived from the periodicity of all columnar elements reported for a region, including cell bodies, axon bundles and dendrites. Data are from published findings on adult humans (excluding Down’s syndrome) Brodmann area
Spacing (lm)
No. of studies
Mean spacing (lm)
Region name
Hierarchical role
Studies
38 21 20 41 42
30 30–86 23–30 46–75 45–83
1 2 2 2 2
30 58 26.5 60.5 64
Inferior temporal cortex
Del Rio & DeFelipe 199717 Del Rio & DeFelipe 199717; Chance et al. 200620 Del Rio & DeFelipe 199717; Di Rosa et al. 200621 Seldon 198126; Chance et al. 200620
22
34–83
6
60
25
50–60
1
55
General sensory association cortex Auditory projection cortex Auditory association cortex Limbic and Prelimbic Cortex
32,32’
50–60
1
55
23 24 31 7
40 40–73* 40 40–80
1 2 1 2
40 56.5 40 60
19
35–40
2
37.5
Posterior parietal lobe
17
16–80
3
40
Occipital lobe
9
70
1
70
Premotor cortex
4
80
1
80
Precentral gyrus
40
80
1
80
Supramarginal lobe
*
Middle 1/3 of Superior Temporal Cortex Superior temporal gyrus Sub genual cingulate Dorsal pregenual anterior cingulate Posterior cingulate Anterior cingulate Precuneus Superior parietal lobule
Buldyrev et al. 200022; Buxhoeveden et al. 200123; Buxhoeveden et al 199624; Casanova et al. 200225; Chance et al. 200620; Seldon 198126 Gabbott et al. 20039 Gabbott et al. 20039
Parietal cortex General sensory association cortex Visual association cortex Visual projection cortex Motor association cortex (dlpfc) Primary motor cortex Somatosensory association cortex
Schlaug et al. 19957 Schlaug et al. 19957; DiRosa et al.* Schlaug et al. 19957 VonBonin & Mehler 197127; Schlaug et al. 19957
Kenan-Vaknin et al. 199218; Schlaug et al 19957
Buxhoeveden et al. 19968; VonBonin & Mehler 197127; Morgane et al. 198828 Casanova et al. 200710
VonBonin & Mehler 197127 VonBonin & Mehler 197128
=current study.
ciation cortex, 56 lm; parieto-occipito-temporal junction (Wernicke’s area), 68 lm. These data suggest a regional hierarchy of organisation of axon bundles and minicolumns in the human brain. Notwithstanding variation in the degree of columnarity20, it is found increasingly that the distribution of minicolumn spacing is 20–90 lm. In measuring cell body arrangement, as well as axon and dendrite bundles, the mean spacing across many studies converges on the range 50–60 lm. References 1. Jespersen SN, Kroenke CD, Ostergaard L, et al. Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage 2007;34:1473–86. 2. Jones EG. Minicolumns in the cerebral cortex. Proc Natl Acad Sci USA 2000;97:5019–21. 3. Szeszko PR, Ardekani BA, Ashtari M, et al. White matter abnormalities in obsessive-compulsive disorder: a diffusion tensor imaging study. Arch Gen Psychiatry 2005;62:782–90. 4. Bae JN, MacFall JR, Krishnan KR, et al. Dorsolateral prefrontal cortex and anterior cingulate cortex white matter alterations in latelife depression. Biol Psychiatry 2006;60:1356–63.
5. McCullumsmith D, Gupta M, Beneyto E, et al. Expression of transcripts for myelination-related genes in the anterior cingulate cortex in schizophrenia? Schizophrenia Research 2007;90:15–27 R. 6. Arikuni T, Sakai M, Kubota K. Columnar aggregation of prefrontal and anterior cingulate cortical cells projecting to the thalamic mediodorsal nucleus in the monkey. J Comp Neurol 1983;220:116–25. 7. Schlaug G, Schleicher A, Zilles K. Quantitative analysis of the columnar arrangement of neurons in the human cingulate cortex. J Comp Neurol 1995;351:441–52. 8. Gabbott PL, Bacon SJ. The organization of dendritic bundles in the prelimbic cortex (area 32) of the rat. Brain Res 1996;730:75–86. 9. Gabbott PL. Radial organization of neurons and dendrites in human cortical areas 25, 32, and 32’D. P Brain Research 2003;992:298–304. 10. Casanova MF, Switala AE, Trippe J. A comparison study of the vertical bias of pyramidal cells in the hippocampus and neocortex. Dev Neurosci 2007;29:193–200. 11. Quester R, Schroder R. The shrinkage of the human brain stem during formalin fixation and embedding in paraffin. J Neurosci Methods 1997;75:81–9. 12. McDonald B, Highley JR, Walker MA, et al. Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: A postmortem study. Am J Psychiatry 2000;157:40–7. 13. Chance SA, Highley JR, Esiri MM, et al. Fiber content of the fornix in schizophrenia: lack of evidence for a primary limbic encephalopathy. Am J Psych 1999;156:1720–4.
1392
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14. Bancroft J, Stevens A, Theory and practice of histological techniques, ISBN: 0-443-04760-X, Churchill Livingstone. 1996. 15. Murray M, Wang SD, Goldberger ME, et al. Modification of astrocytes in the spinal cord following dorsal root or peripheral nerve lesions. Exp Neurol 1990;110:248–57. 16. Favorov OV, Kelly DG. Minicolumnar organization within somatosensory cortical segregates: II. Emergent functional properties. Cereb Cortex 1994;4:428–42. 17. Del Rio MR, DeFelipe J. Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J Chem Neuroanat 1997;13:243–51. 18. Kenan-Vaknin G, Ouaknine GE, Razon N, et al. Organization of layers II–III connections in human visual cortex revealed by in vitro injections of biocytin. Brain Res 1992;594:339–42. 19. Benes FM, Bird ED. An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Arch Gen Psychiatry 1987;44:608–16. 20. Chance SA, Casanova MF, Switala AE, et al. Minicolumn thinning in temporal lobe association cortex but not primary auditory cortex in normal human ageing. Acta Neuropathol (Berl) 2006;111:459–64.
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