Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-13T05:09:41.377Z Has data issue: false hasContentIssue false
  • English
  • Français

Resolving the organization of the territory of the third visual area: A new proposal

Published online by Cambridge University Press:  27 July 2015

JON H. KAAS ,
ANNA W. ROE ,
MARY K.L. BALDWIN  and
DAVID C. LYON
JON H. KAAS*
Affiliation:
Department of Psychology, Vanderbilt University, Nashville, Tennessee
ANNA W. ROE
Affiliation:
Department of Psychology, Vanderbilt University, Nashville, Tennessee
MARY K.L. BALDWIN
Affiliation:
Center for Neuroscience, University of California, Davis, Davis, California
DAVID C. LYON
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, California
*
*Address correspondence to: Jon H. Kaas, Department of Psychology, Vanderbilt University, 111 21st Avenue S., Nashville, TN 37240-7817. E-mail: jon.h.kaas@vanderbilt.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

In primates, the cortex adjoining the rostral border of V2 has been variously interpreted as belonging to a single visual area, V3, with dorsal V3 (V3d) representing the lower visual quadrant and ventral V3 (V3v) representing the upper visual quadrant, V3d and V3v constituting separate, incomplete visual areas, V3d and ventral posterior (VP), or V3d being divided into several visual areas, including a dorsomedial (DM) visual area, a medial visual area (M), and dorsal extension of VP (or VLP). In our view, the evidence from V1 connections strongly supports the contention that V3v and V3d are parts of a single visual area, V3, and that DM is a separate visual area along the rostral border of V3d. In addition, the retinotopy revealed by V1 connection patterns, microelectrode mapping, optical imaging mapping, and functional magnetic resonance imaging (fmri) mapping indicates that much of the proposed territory of V3d corresponds to V3. Yet, other evidence from microelectrode mapping and anatomical connection patterns supports the possibility of an upper quadrant representation along the rostral border of the middle of dorsal V2 (V2d), interpreted as part of DM or DM plus DI, and along the midline end of V2d, interpreted as the visual area M. While the data supporting these different interpretations appear contradictory, they also seem, to some extent, valid. We suggest that V3d may have a gap in its middle, possibly representing part of the upper visual quadrant that is not part of DM. In addition, another visual area, M, is likely located at the DM tip of V3d. There is no evidence for a similar disruption of V3v. For the present, we favor continuing the traditional concept of V3 with the possible modification of a gap in V3d in at least some primates.

Keywords

PrimatesVisual cortexArea 17Area V3Vision
Type
Perspective
Information
Visual Neuroscience , Volume 32 , 2015 , E016
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdollahi, R.O., Kolter, H., Glasser, M.F., Robinson, E.C., Coalson, T.S., Dierker, D.L., Joenkinson, M., Van Essen, D.C. & Orban, G.A. (2014). Correspondence between retinotopic areas and myelin maps in human visual cortex. NeuroImage 99, 509–524.CrossRefGoogle ScholarPubMed
Allman, J.M., Campbell, C.B. & McGuinness, E.R. (1979). The dorsal third tier area in Galago senegalensis. Brain Research 179, 355–361.CrossRefGoogle ScholarPubMed
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, 473–487.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1976). Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. Science 191, 572–575.CrossRefGoogle ScholarPubMed
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). The Journal of Comparative Neurology 400, 18–34.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Beck, P.D. & Kaas, J.H. (1999). Cortical connections of the dorsomedial visual area in Old World macaque monkeys. The Journal of Comparative Neurology 406, 487–502.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Brewer, A.A., Press, W.A., Logothetis, N.K. & Wandell, B.A. (2002). Visual areas in macaque cortex measured using functional magnetic resonance imaging. The Journal of Neuroscience 22, 10416–10426.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrhinde. [Comparative Localization Theory of the Cerebral Cortex]. Leipzig, Barth. Germany.Google Scholar
Burkhalter, A., Felleman, D.J., Newsome, W.T. & Van Essen, D.C. (1986). Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex. Vision Research 26, 63–80.CrossRefGoogle ScholarPubMed
Burkhalter, A. & Van Essen, D.C. (1986). Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey. The Journal of Neuroscience 6, 2327–2351.CrossRefGoogle ScholarPubMed
Colby, C.L., Gattass, R., Olson, C.R. & Gross, C.G. (1988). Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: A dual tracer study. The Journal of Comparative Neurology 269, 392–413.CrossRefGoogle ScholarPubMed
Cragg, B.C. (1969). The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. Vision Research 9, 733–747.CrossRefGoogle ScholarPubMed
Fan, R.H., Baldwin, M.K., Jermakowicz, W.J., Casagrande, V.A., Kaas, J.H. & Roe, A.W. (2012). Intrinsic signal optical imaging evidence for dorsal V3 in the prosimian galago (Otolemur garnettii). The Journal of Comparative Neurology 520, 4254–4274.CrossRefGoogle ScholarPubMed
Felleman, D.J., Burkhalter, A. & Van Essen, D.C. (1997). Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex. The Journal of Comparative Neurology 379, 21–47.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1987). Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. Journal of Neurophysiology 57, 889–920.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 1–47.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. The Journal of Neuroscience 8, 1831–1845.CrossRefGoogle ScholarPubMed
Grill-Spector, K. & Malach, R. (2004). The human visual cortex. Annual Review of Neuroscience 27, 649–677.CrossRefGoogle ScholarPubMed
Hof, P.R. & Morrison, J.H. (1995). Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. The Journal of Comparative Neurology 352, 161–186.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965). Receptive fields and functional architecture in two nonstraite visual areas (18 and 19) of the cat. Journal of Neurophysiology 30, 1561–1573.CrossRefGoogle Scholar
Jeffs, J., Federer, F., Ichida, J.M. & Angelucci, A. (2013). High-resolution mapping of anatomical connections in marmoset extrastriate cortex reveals a complete representation of the visual field bordering dorsal V2. Cerebral Cortex 23, 1126–1147.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1993a). Evolution of multiple areas and modules within neocortex. Perspectives on Developmental Neurobiology 1, 101–107.Google ScholarPubMed
Kaas, J.H. (1993b). The organization of visual cortex in primates: Problems, conclusions, and the use of comparative studies in understanding the human brain. In The Functional Organization of the Human Visual Cortex, ed. Gulás, B., Ottoson, D. & Roland, P.E., pp. 1–14. Oxford: Pergamon Press.Google Scholar
Kaas, J.H. (1997). Theories of visual cortex organization in primates. In Cerebral Cortex: Extrastriate Cortex in Primates, ed. Rockland, K.S., Kaas, J.H. & Peters, A., pp. 91–125. New York: Plenum Press.CrossRefGoogle Scholar
Kaas, J.H. (2005a). The evolution of visual cortex in primates. In The Structure, Function and Evolution of the Primate Visual System, ed. Kremers, J., Chichester, UK: John Wiley and Sons.Google Scholar
Kaas, J.H. (2005b). The future of mapping sensory cortex in primates: Three of many remaining issues. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 653–664.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Lyon, D.C. (2001). Visual cortex organization in primates: Theories of V3 and adjoining visual areas. Progress in Brain Research 134, 285–295.CrossRefGoogle ScholarPubMed
Kaskan, P.M., Lu, H.D., Dillenburger, B.C., Kaas, J.H. & Roe, A.W. (2009). The organization of orientation-selective, luminance-change and binocular-preference domains in the second (V2) and third (V3) visual areas of New World owl monkeys as revealed by intrinsic signal optical imaging. Cerebral Cortex 19, 1394–1407.CrossRefGoogle ScholarPubMed
Kolster, H., Mandeville, J.B., Arsenault, J.T., Ekstrom, L.B., Wald, L.L. & Vanduffel, W. (2009). Visual field map clusters in macaque extrastriate visual cortex. The Journal of Neuroscience 29, 7031–7039.CrossRefGoogle ScholarPubMed
Kolster, H., Peeters, R. & Orban, G.A. (2010). The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. The Journal of Neuroscience 30, 9801–9820.CrossRefGoogle ScholarPubMed
Konorski, M.D. (1967). Integrative Activity of the Brain. Chicago: University of Chicago Press.Google Scholar
Krubitzer, L.A. & Kaas, J.H. (1990). Convergence of processing channels in the extrastriate cortex of monkeys. Visual Neuroscience 5, 609–613.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1993). The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates. The Journal of Comparative Neurology 334, 497–528.CrossRefGoogle ScholarPubMed
Larsson, J. and Heeger, D.J. (2006). Two retinotopic visual areas in human lateral occipital cortex. The Journal of Neuroscience 26, 13128–13142.CrossRefGoogle ScholarPubMed
Lui, L.L., Bourne, J.A. & Rosa, M.G.P. (2006). Functional response properties of neurons in the dorsomedial visual area of New World monkeys (callithrix jacchus). Cerebral Cortex 16, 162–177.CrossRefGoogle ScholarPubMed
Lyon, D.C. (2013). The case for a dorsal V3 in the “third tier” of primate visual cortex: A reply to “the case for a dorsomedial area in the primate ‘third-tier’ visual cortex”. Proceedings of the Royal Society B: Biological Sciences 280, Comments & Invited Replies. 20121994; Published 21 November 2012. doi: 10.1098/rspb.2012.1994.Google Scholar
Lyon, D.C. & Connolly, J.D. (2012). The case for primate V3. Proceedings. Biological Sciences / The Royal Society 279, 625–633.CrossRefGoogle ScholarPubMed
Lyon, D.C. & Kaas, J.H. (2001). Connectional and architectonic evidence for dorsal and ventral V3, and dorsomedial area in marmoset monkeys. The Journal of Neuroscience 21, 249–261.CrossRefGoogle ScholarPubMed
Lyon, D.C. & Kaas, J.H. (2002a). Connectional evidence for dorsal and ventral V3, and other extrastriate areas in the prosimian primate, Galago garnetti. Brain, Behavior and Evolution 59, 114–129.CrossRefGoogle ScholarPubMed
Lyon, D.C. & Kaas, J.H. (2002b). Evidence for a modified V3 with dorsal and ventral halves in macaque monkeys. Neuron 33, 453–461.CrossRefGoogle ScholarPubMed
Lyon, D.C. & Kaas, J.H. (2002c). Evidence from V1 connections for both dorsal and ventral subdivisions of V3 in three species of New World monkeys. The Journal of Comparative Neurology 449, 281–297.CrossRefGoogle ScholarPubMed
Lyon, D.C., Xu, X., Casagrande, V.A., Stefansic, J.D., Shima, D. & Kaas, J.H. (2002). Optical imaging reveals retinotopic organization of dorsal V3 in New World owl monkeys. Proceedings of the National Academy of Sciences of the United States of America 99, 15735–15742.CrossRefGoogle ScholarPubMed
Myers, R.E. (1965). Organization of visual pathways. In Functions of the Corpus Callosum, ed. Ettlinger, E.G., pp. 133. Churchill: London.Google Scholar
Nakamura, H., Le, W.R., Wakita, M., Mikami, A. & Itoh, K. (2004). Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque. Experimental Brain Research 155, 102–110.CrossRefGoogle Scholar
Neuenschwander, S., Gattass, R., Sousa, A.P.B. & Piñon, M.C.G. (1994). Identification and visuotopic organization of areas PO and POd in Cebus monkey. The Journal of Comparative Neurology 340, 65–86.CrossRefGoogle ScholarPubMed
Newsome, W.T. & Allman, J.M. (1980). Interhemispheric connections of visual cortex in the owl monkey, Aotus trivirgatus, and the bushbaby, Galago senegalensis. The Journal of Comparative Neurology 194, 209–233.CrossRefGoogle ScholarPubMed
Newsome, W.T., Maunsell, J.H.R. & Van Essen, D.C. (1986). Ventral visual area of the macaque: Visual topography and area boundaries. The Journal of Comparative Neurology 252, 139–153.CrossRefGoogle Scholar
Orban, G.A., Van Essen, D. & Vanduffel, W. (2004). Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Sciences 8, 315–324.CrossRefGoogle ScholarPubMed
Otsuka, R. & Hassler, R. (1962). Uber Aufbau und Gliederung der corticalen Shesphäre bei der katzs. Arch Psychiat Nervenkri 303, 212–234.CrossRefGoogle Scholar
Perkel, D.J., Bullier, J. & Kennedy, H. (1986). Topography of the afferent connectivity of area 17 in the macaque monkey: A double-labelling study. Journal of Comparative Neurology 253, 374–402.CrossRefGoogle ScholarPubMed
Previc, F.H. (1990). Functional specialization in the lower and upper visual fieldsin humans: Its ecological origins and neurophysiological implications. The Behavioral and Brain Sciences 13, 519–575.CrossRefGoogle Scholar
Rockland, K.S. & Pandya, D.N. (1979). Laminar origins and terminations of cortical connections to the occipital lobe in the rhesus monkey. Brain Research 179, 3–20.CrossRefGoogle Scholar
Rosa, M.G. & Schmid, L.M. (1995). Visual areas in the dorsal and medial extrastriate cortices of the marmoset. The Journal of Comparative Neurology 359(2), 272–299.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Casagrande, V.A., Preuss, T.M. & Kaas, J.H. (1997). Visual field representation in striate and prestriate cortices of a prosimian primate (Galago garnettii). Journal of Neurophysiology 77, 3193–3217.CrossRefGoogle Scholar
Rosa, M.G.P. & Manger, P.R. (2005). Clarifying homologies in the mammalian cerebral cortex: The case of the third visual area (V3). Clinical and Experimental Pharmacology & Physiology 32, 327–339.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Palmer, S.M., Gamberini, M., Berman, K.J., Yu, H.H., Reser, D.H., Bourne, J.A., Tweedale, R. & Galletti, C. (2009). Connections of the dorsomedial visual area: Pathways for early integration of dorsal and ventral streams in extrastriate cortex. The Journal of Neuroscience 29, 4548–4563.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Palmer, S.M., Gamberini, M., Tweedale, R., Pinon, M.C.G. & Bourne, J.A. (2005). Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus). The Journal of Comparative Neurology 483, 164–191.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Piñon, M.C., Gattass, R. & Sousa, A.P.B. (2000). “Third tier” ventral extrastriate cortex in the New World monkey, Cebus apella. Experimental Brain Research 132, 287–305.CrossRefGoogle ScholarPubMed
Rosa, M.G.P. & Tweedale, R. (2000). Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey. The Journal of Comparative Neurology 422, 621–651.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Rosa, M.G.P. & Tweedale, R. (2001). The dorsomedial visual areas in New World and Old World monkeys: homology and function. The European Journal of Neuroscience 13, 421–427.CrossRefGoogle ScholarPubMed
Rosa, M.G.P. & Tweedale, R. (2005). Brain maps, great and small: Lessions from comparative studies of primate visual cortical organization. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 665–691.CrossRefGoogle Scholar
Rottschy, C., Eickhoff, S.B., Schleicher, A., Mohiberg, H., Kujovic, M., Zilles, K. & Amunts, K. (2007). Ventral visual cortex in humans: Cytoarchitectonic mapping of two extrastriate areas. Human Brain Mapping 28, 1045–1059.CrossRefGoogle ScholarPubMed
Sousa, A.P.B., Piñon, M.C.G., Gattass, R. & Rosa, M.G.P. (1991). Topographic organization of cortical input to striate cortex in the Cebus monkey: A fluorescent tracer study. The Journal of Comparative Neurology 308, 665–682.CrossRefGoogle ScholarPubMed
Spatz, W.B. & Tigges, J. (1972). Species difference between Old World and New World monkeys in the organization of the striate-prestriate association. Brain Research 43, 591–594.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Mendola, J.D., Hadjikani, N.K., Ledden, P.J., Liu, A.K., Reppas, J.B., Sereno, M.I. & Dale, A.M. (1997). Functional analysis of V3A and related areas in human visual cortex. The Journal of Neuroscience 17, 7060–7078.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Nelissen, K., Vanduffel, W. & Orban, G.A. (2004). Search for color "center(s)" in macaque visual cortex. Cerebral Cortex 14, 353–363.CrossRefGoogle Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. The Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Van Essen, D.C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318.CrossRefGoogle ScholarPubMed
Van Essen, D.C., Newsome, W.T., Maunsell, J.H.R. & Bixby, J.L. (1986). The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections. The Journal of Comparative Neurology 244, 451–480.CrossRefGoogle ScholarPubMed
Vanduffel, W., Zhu, Q. & Orban, G.A. (2014). Monkey cortex through fMRI glasses. Neuron 83, 533–550.CrossRefGoogle ScholarPubMed
von Economo, C. (1929). The Cytoarchitectonics of the Human Cortex. Oxford: Oxford University Press.Google Scholar
Wade, A.R., Brewer, A.A., Rieger, J.W. & Wandell, B.A. (2002). Functional measurements of human functional ventral occipital cortex: Retinotopy and color. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 963–973.CrossRefGoogle Scholar
Wilson, M.E. (1968). Cortico-cortical connections of the cat visual areas. Journal of Anatomy 102, 378–386.Google ScholarPubMed
Xu, X., Bosking, W.H., Sary, G., Stefansic, J.D., Shima, D. & Casagrande, V. (2004). Functional organization of visual cortex in the owl monkey. The Journal of Neuroscience 24, 6237–6247.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1969). Representation of central visual fields in prestriate cortex of monkey. Brain Research 14, 271–291.CrossRefGoogle ScholarPubMed
Zeki, S.M. (2004). Improbable areas in color vision. In The Visual Neurosicences, ed. Werner, J.S. & Chalupa, L.M., pp. 1029–1039. Cambridge: MIT Press.Google Scholar
Zeki, S.M. (1971). Cortical projections from two prestriate areas in the monkey. Brain Research 19, 63–75.CrossRefGoogle Scholar