Skip to main content Accessibility help
×
Home

Complete flatmounting of the macaque cerebral cortex

  • LAWRENCE C. SINCICH (a1), DANIEL L. ADAMS (a1) and JONATHAN C. HORTON (a1)

Abstract

The elaborate folding of the brain surface has posed a practical impediment to investigators engaged in mapping the areas of the cerebral cortex. This obstacle has been overcome partially by the development of methods to erase the sulci and gyri by physically flattening the cortex prior to sectioning. In this study, we have prepared a step-by-step atlas of the flatmounting process for the entire cerebral cortex in the macaque monkey. The cortex was dissected from the white matter, unfolded, and flattened in a single piece of tissue by making three relieving cuts. The flatmount was sectioned at 60–75 μm and processed for cytochrome oxidase (CO) or myelin. From animal to animal there was nearly a twofold variation in the surface area of individual cortical regions, and of the whole cortex. In each specimen, a close correlation was found between V1 surface area (mean = 1343 mm2), V2 surface area (mean = 1012 mm2), hippocampal area (mean = 181 mm2), and total cerebral cortex area (mean = 10,430 mm2). The complete pattern of CO stripes in area V2 was labeled clearly in several cases; the number of cycles of thick-pale-thin-pale stripes ranged from 26 to 34. Characteristic patterns of strong CO activity were encountered in areas V3, MT, auditory and somatosensory cortex. In some animals we made injections of a retrograde tracer, gold-conjugated cholera toxin B subunit, into area V2 to identify all sources of cortical input. In addition to previously described inputs, we identified three new regions in the occipitotemporal region that project to V2. Flatmounting the cerebral cortex is a simple, efficient method that can be used routinely for mapping areas and connections in the macaque brain, the most widely used primate model of the human brain.

Copyright

Corresponding author

Address correspondence and reprint requests to: Jonathan C. Horton, Beckman Vision Center, University of California—San Francisco, 10 Koret Way, San Francisco, CA 94143-0730, USA. E-mail: horton@itsa.ucsf.edu

References

Hide All

REFERENCES

Adams, D.L. & Horton, J.C. (2003). Capricious expression of cortical columns in the primate brain. Nature Neuroscience 6, 113114.
Allman, J.M. & Kaas, J.H. (1971). A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Research 31, 85105.
Allman, J.M. & Kaas, J.H. (1974). The organization of the second visual area (V II) in the owl monkey: A second order transformation of the visual hemifield. Brain Research 76, 247265.
Allman, J.M. & Kaas, J.H. (1975). The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). Brain Research 100, 473487.
Anderson, J.C. & Martin, K.A.C. (2002). Connection from cortical area V2 to MT in macaque monkey. Journal of Comparative Neurology 443, 5670.
Andrews, T.J., Halpern, S.D., & Purves, D. (1997). Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. Journal of Neuroscience 17, 28592868.
Beck, P.D. & Kaas, J.H. (1998). Cortical connections of the dorsomedial visual area in new world owl monkeys (Aotus trivirgatus) and squirrel monkeys (Saimiri sciureus). Journal of Comparative Neurology 400, 1834.
Beck, P.D. & Kaas, J.H. (1999). Cortical connections of the dorsomedial visual area in old world macaque monkeys. Journal of Comparative Neurology 406, 487502.
Boyd, J.D. & Casagrande, V.A. (1999). Relationships between cytochrome oxidase (CO) blobs in primate primary visual cortex (V1) and the distribution of neurons projecting to the middle temporal area (MT). Journal of Comparative Neurology 409, 573591.
Brewer, A.A., Press, W.A., Logothetis, N.K., & Wandell, B.A. (2002). Visual areas in macaque cortex measured using functional magnetic resonance imaging. Journal of Neuroscience 22, 1041610426.
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: J. A. Barth.
Brodmann, K. (1918). Individuelle Variationen der Sehsphäre und ihr Bedeutung für die Klinik der Hinterhauptschüsse. Allgz Psychiat (Berlin) 74, 564568.
Clarke, S. & Rivier, F. (1998). Compartments within human primary auditory cortex: Evidence from cytochrome oxidase and acetylcholinesterase staining. European Journal of Neuroscience 10, 741745.
Collins, C.E., Stepniewska, I., & Kaas, J.H. (2001). Topographic patterns of V2 cortical connections in a prosimian primate (Galago garnetti). Journal of Comparative Neurology 431, 155167.
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9, 179194.
Desimone, R. & Ungerleider, L.G. (1986). Multiple visual areas in the caudal superior temporal sulcus of the macaque. Journal of Comparative Neurology 248, 164189.
De Vries, I. (1912). Über die Zytoarchitektonik der Grosshirnrinde der Maus und über die Beziehungen der einzelnen Zellschichten zum Corpus Callosum auf Grund von experimentellen Läsionen. Folia neuro-biol 6, 288322.
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317, 5861.
Droogleever Fortuyn, A.B. (1914). Cortical cell-lamination of the hemispheres of some rodents. Archives of Neurology and Psychiatry (Mott's) 6, 221354.
Drury, H.A., Van Essen, D.C., Anderson, C.H., Lee, C.W., Coogan, T.A., & Lewis, J.W. (1996). Computerized mappings of the cerebral cortex: A multiresolution flattening method and a surface-based coordinate system. Journal of Cognitive Neuroscience 8, 128.
Eskenasy, A.C. & Clarke, S. (2000). Hierarchy within human SI: Supporting data from cytochrome oxidase, acetylcholinesterase and NADPH-diaphorase staining patterns. Somatosensory and Motor Research 17, 123132.
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 147.
Felleman, D.J., Xiao, Y., & McClendon, E. (1997). Modular organization of occipito-temporal pathways: Cortical connections between visual area 4 and visual area 2 and posterior inferotemporal ventral area in macaque monkeys. Journal of Neuroscience 17, 31853200.
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195207.
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203209.
Gattass, R. & Gross, C.G. (1981). Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 621638.
Gattass, R., Sousa, A.P., Mishkin, M., & Ungerleider, L.G. (1997). Cortical projections of area V2 in the macaque. Cerebral Cortex 7, 110129.
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199253.
Horton, J.C. & Hocking, D.R. (1996). Intrinsic variability of ocular dominance column periodicity in normal macaque monkeys. Journal of Neuroscience 16, 72287239.
Horton, J.C. & Hocking, D.R. (1997). Myelin patterns in V1 and V2 of normal and monocularly enucleated monkeys. Cerebral Cortex 7, 166177.
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762764.
Hubel, D.H. & Wiesel, T.N. (1969). Anatomical demonstration of columns in the monkey striate cortex. Nature 221, 747750.
Jones, E.G., Dell'Anna, M.E., Molinari, M., Rausell, E., & Hashikawa, T. (1995). Subdivisions of macaque monkey auditory cortex revealed by calcium-binding protein immunoreactivity. Journal of Comparative Neurology 362, 153170.
Jones, E.G., Woods, T.M., & Manger, P.R. (2002). Adaptive responses of monkey somatosensory cortex to peripheral and central deafferentation. Neuroscience 111, 775797.
Kennedy, H. & Bullier, J. (1985). A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. Journal of Neuroscience 5, 28152830.
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. Visual Neuroscience 5, 165204.
Krubitzer, L.A. & Kaas, J.H. (1993). The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates. Journal of Comparative Neurology 334, 497528.
LeVay, S., Connolly, M., Houde, J., & Van Essen, D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486501.
Lewis, J.W. & Van Essen, D.C. (2000). Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. Journal of Comparative Neurology 428, 79111.
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309356.
Llewellyn-Smith, I.J., Minson, J.B., Wright, A.P., & Hodgson, A.J. (1990). Cholera toxin B-gold, a retrograde tracer that can be used in light and electron microscopic immunocytochemical studies. Journal of Comparative Neurology 294, 179191.
Lorente De Nó, R. (1922). La corteza cerebral del ratón. Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid 20, 4178.
Lyon, D.C. & Kaas, J.H. (2001). Connectional and architectonic evidence for dorsal and ventral V3, and dorsomedial area in marmoset monkeys. Journal of Neuroscience 21, 249261.
Lyon, D.C. & Kaas, J.H. (2002). Evidence for a modified v3 with dorsal and ventral halves in macaque monkeys. Neuron 33, 453461.
Maunsell, J.H.R. & Van Essen, D.C. (1987). Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535555.
Mouritzen Dam, A. (1979). Shrinkage of the brain during histological procedures with fixation in formaldehyde solutions of different concentrations. Journal of Hirnforsch 20, 115119.
Olavarria, J.F. & Van Sluyters, R.C. (1985). Unfolding and flattening the cortex of gyrencephalic brains. Journal of Neuroscience Methods 15, 191202.
Olavarria, J.F. & Van Essen, D.C. (1997). The global pattern of cytochrome oxidase stripes in visual area V2 of the macaque monkey. Cerebral Cortex 7, 395404.
Penfield, W. & Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389443.
Piccolomini, A. (1586). Anatomicae praelectiones explicantes mirificam corporis humani fabricam (Rome). Translated in E. Clarke and C.D. O'Malley, The Human Brain and Spinal Cord, San Francisco: Norman Publishing, pp. 387–388.
Preuss, T.M., Beck, P.D., & Kaas, J.H. (1993). Areal, modular, and connectional organization of visual cortex in a prosimian primate, the slow loris (Nycticebus coucang). Brain, Behavior and Evolution 42, 321335.
Rockland, K.S. & Pandya, D.N. (1979). Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research 179, 320.
Rockland, K.S. & Van Hoesen, G.W. (1994). Direct temporal-occipital feedback connections to striate cortex (V1) in the macaque monkey. Cerebral Cortex 4, 300313.
Roe, A.W. & Ts'o, D.Y. (1999). Specificity of color connectivity between primate V1 and V2. Journal of Neurophysiology 82, 27192730.
Rose, M. (1912). Histologische Lokalisation der Grosshirnrinde bei kleinen Säugetieren (Rodentia, Insectivora, Chiroptera). Journal für Psychologie und Neurologie (Leipzig) 19, 389479.
Rovamo, J. & Virsu, V. (1984). Isotropy of cortical magnification and topography of striate cortex. Vision Research 24, 283286.
Sereno, M.I., Dale, A.M., Reppas, J.B., Kwong, K.K., Belliveau, J.W., Brady, T.J., Rosen, B.R., & Tootell, R.B. (1995). Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889893.
Sherk, H. (1992). Flattening the cerebral cortex by computer. Journal of Neuroscience Methods 41, 255267.
Sincich, L.C. & Horton, J.C. (2002a). Divided by cytochrome oxidase: A map of the projections from V1 to V2 in macaques. Science 295, 17341737.
Sincich, L.C. & Horton, J.C. (2002b). Pale cytochrome oxidase stripes in V2 receive the richest projection from macaque striate cortex. Journal of Comparative Neurology 447, 1833.
Stensaas, S.S., Eddington, D.K., & Dobelle, W.H. (1974). The topography and variability of the primary visual cortex in man. Journal of Neurosurgery 40, 747755.
Stepniewska, I. & Kaas, J.H. (1996). Topographic patterns of V2 cortical connections in macaque monkeys. Journal of Comparative Neurology 371, 129152.
Tootell, R.B. & Silverman, M.S. (1985). Two methods for flat-mounting cortical tissue. Journal of Neuroscience Methods 15, 177190.
Tootell, R.B., Silverman, M.S., Switkes, E., & De Valois, R.L. (1982). Deoxyglucose analysis of retinotopic organization in primate striate cortex. Science 218, 902904.
Tootell, R.B., Hamilton, S.L., & Silverman, M.S. (1985). Topography of cytochrome oxidase activity in owl monkey cortex. Journal of Neuroscience 5, 27862800.
Tootell, R.B.H. & Taylor, J.B. (1995). Anatomical evidence for MT and additional cortical visual areas in humans. Cerebral Cortex 1, 3955.
Tootell, R.B.H., Silverman, M.S., De Valois, R.L., & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737739.
Van Essen, D.C. (2003). Organization of visual areas in macaque and human cerebral cortex. In Visual Neurosciences, ed. Werner, J.S. & Chalupa, L.M., pp. 507522. Cambridge, Massachusetts: MIT Press.
Van Essen, D.C. & Zeki, S.M. (1978). The topographic organization of rhesus monkey prestriate cortex. Journal of Physiology 277, 193226.
Van Essen, D.C. & Maunsell, J.H.R. (1980). Two-dimensional maps of the cerebral cortex. Journal of Comparative Neurology 191, 255281.
Van Essen, D.C., Maunsell, J.H.R., & Bixby, J.L. (1981). The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties and topographic organization. Journal of Comparative Neurology 199, 293326.
Van Essen, D.C., Newsome, W.T., & Maunsell, J.H. (1984). The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability. Vision Research 24, 429448.
Van Essen, D.C., Lewis, J.W., Drury, H.A., Hadjikhani, N., Tootell, R.B., Bakircioglu, M., & Miller, M.I. (2001). Mapping visual cortex in monkeys and humans using surface-based atlases. Vision Research 41, 13591378.
Welker, C. & Woolsey, T.A. (1974). Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse. Journal of Comparative Neurology 158, 437453.
Wong-Riley, M. & Carroll, E.W. (1984). Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262264.
Woolsey, T.A. & Van Der Loos, H. (1970). The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex: The description of a cortical field composed of cytoarchitectonic units. Brain Research 17, 205242.
Zeki, S.M. (1978). The third visual complex of rhesus monkey prestriate cortex. Journal of Physiology 277, 245272.

Keywords

Related content

Powered by UNSILO

Complete flatmounting of the macaque cerebral cortex

  • LAWRENCE C. SINCICH (a1), DANIEL L. ADAMS (a1) and JONATHAN C. HORTON (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.