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Divergent feedback connections from areas V4 and TEO in the macaque

Published online by Cambridge University Press:  02 June 2009

Kathleen S. Rockland ,
Kadharbatcha S. Saleem  and
Keiji Tanaka
Kathleen S. Rockland
Affiliation:
Department of Neurology, University of Iowa, Iowa City
Kadharbatcha S. Saleem
Affiliation:
Laboratory for Neural Information Processing, Frontier Research Program, Saitama 351–01, Japan
Keiji Tanaka
Affiliation:
Laboratory for Neural Information Processing, Frontier Research Program, Saitama 351–01, Japan Information Science Laboratory, The Institute of Physical and Chemical Research (RIKEN), Saitama 351–01, Japan
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Abstract

Extrastriate areas TEO and V4 have been associated with form and color vision. Area V4 has also been suggested to participate in processes concerned with attention, stimulus salience, and perceptual learning. In a continuing effort to elucidate the connectional interactions and microcircuitry of these areas, we describe in this report the pattern of feedback connections from TEO and V4. Connections were demonstrated by injections of the high-resolution anterograde tracers PHA-L or biocytin and further analyzed by reconstruction of 25 individual axons through serial sections. This analysis yielded several new results: (1) Both areas TEO and V4 have widespread feedback connections (defined by their preferential termination in layer 1 and avoidance of layer 4). From TEO, there are dense projections to area V4 and moderate ones to V2 and V1. From V4, there are dense projections to V2 and moderate ones to V3 and V1. (2) Terminal fields span large territories in area V1, up to 6.0 mm in the case of axons originating from TEO; up to 5.0 mm in the case of axons originating from V4. In V2, fields tend to be smaller, between 3.0–5.0 mm. (3) Many axons from TEO and some from V4 have terminations in both areas V1 and V2. (4) Because individual terminal clusters and segments are often larger than cytochrome oxidase compartments, especially in V1, we suggest they may not be correlated with this compartmental organization. These results are consistent with the hypothesis that feedback connections may contribute to processes other than perceptual discrimination.

Keywords

AxonsExtrastriate cortexFeedbackPHA-LV1
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 3 , May 1994 , pp. 579 - 600
Copyright
Copyright © Cambridge University Press 1994

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References

Allman, J.M., Miezin, F. & McGuiness, E. (1985). Stimulus-specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons. Annual Review of Neuroscience 8, 407–430.CrossRefGoogle ScholarPubMed
Amaral, D.G. & Price, J.L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology 230, 465–496.CrossRefGoogle ScholarPubMed
Baizer, J.S., Ungerleider, L.G. & Desimone, R. (1991). Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. Journal of Neuroscience 11, 168–190.CrossRefGoogle Scholar
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle ScholarPubMed
Boussaoud, D., Desimone, R. & Unoerleider, L.G. (1991). Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554–575.CrossRefGoogle ScholarPubMed
Bullier, J., Girard, P. & Salin, P.A. (1993). The role of area 17 in the transfer of information to extrastriate visual cortex. In Cerebral Cortex, Vol. 10, ed. Peters, A. & Rockland, K.S., pp. 301–330. New York: Plenum Press.Google Scholar
Cauller, L.J. & Connors, B.W. (1992). Functions of very distal dendrites: Experimental and computational studies of layer 1 synapses on neocortical pyramidal cells. In Single Neuron Computation, ed. McKenna, T., Davis, J. & Zornetzer, S.F., pp. 199–230. New York: Academic Press.CrossRefGoogle Scholar
Celebrini, S., Thorpe, S., Trotter, Y. & Imbert, M. (1993). Dynamics of orientation coding in area V1 of the awake primate. Visual Neuroscience 10, 811–825.CrossRefGoogle ScholarPubMed
Cusick, C.G. & Kaas, J.H. (1988). Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys. Visual Neuroscience 1, 211–237.CrossRefGoogle ScholarPubMed
Damasio, A.R. (1989). The brain binds entities and events by multi-regional activation from convergence zones. Neural Computation 1, 123–132.CrossRefGoogle Scholar
Damasio, A.R. & Damasio, H. (1993). Cortical systems for retrieval of concrete knowledge: The convergence zone framework. In Large-Scale Neuronal Theories of the Brain, ed. Koch, C., pp. 373–386. Cambridge: MIT Press.Google Scholar
Damasio, H., Grabowski, T.J., Damasio, A., Tranel, D., Boles-Ponto, L., Watkins, G.L. & Hichwa, R.D. (1993). Visual recall with eyes closed and covered activates early visual cortices. Society for Neuroscience Abstracts 19, 1603.Google Scholar
Desimone, R. & Schein, S.J. (1987). Visual properties of neurons in area V4 of the macaque: Sensitivity to stimulus form. Journal of Neurophysiology 57, 835–868.CrossRefGoogle ScholarPubMed
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, 58–61.CrossRefGoogle ScholarPubMed
Distler, C., Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1993). Cortical connections of inferior temporal area TEO in macaque monkeys. Journal of Comparative Neuroscience 334, 125–150.CrossRefGoogle ScholarPubMed
Doty, R.W. (1983). Nongeniculate afferents to striate cortex in macaques. Journal of Comparative Neurology 218, 159–173.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
Freund, T.F., Martin, K.A.C., Soltesz, I., Somogyi, P. & Whit-teridge, D. (1989). Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. Journal of Comparative Neurology 289, 315–336.CrossRefGoogle ScholarPubMed
Gallant, J.L., Braun, J. & Van Essen, D.C. (1993). Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. Science 259, 100–103.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. Journal of Neuroscience 8, 1831–1845.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1993). Circuitry, architecture and functional dynamics of visual cortex. Cerebral Cortex 3, 373–386.CrossRefGoogle ScholarPubMed
Girard, P. & Bullier, J. (1991). Visual activity in macaque area V4 depends on area 17 input. Neuroreport 2, 81–84.CrossRefGoogle ScholarPubMed
Gross, C.G. (1991). Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex. Neuropsychologic 29, 497–515.CrossRefGoogle ScholarPubMed
Haenny, P.E. & Schiller, P.H. (1988). State dependent activity in monkey visual cortex. I. Single cell activity in V1 and V4 on visual tasks. Experimental Brain Research 69, 225–244.CrossRefGoogle ScholarPubMed
Haenny, P.E., Maunsell, H.J.R. & Schiller, P.H. (1988). State dependent activity in monkey visual cortex. II. Retinal and extraretinal factors in V4. Experimental Brain Research 69, 245–259.CrossRefGoogle ScholarPubMed
Heywood, C.A., Gadotti, A. & Cowey, A. (1992). Cortical area V4 and its role in the perception of color. Journal of Neuroscience 12, 4056–4065.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 3378–3415.CrossRefGoogle ScholarPubMed
Iwai, E. & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, M. mulatto, and M. Fascicularis). Journal of Comparative Neurology 261, 362–387.CrossRefGoogle Scholar
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, 2815–2830.CrossRefGoogle ScholarPubMed
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. Journal of Neurophysiology 67, 961–980.CrossRefGoogle ScholarPubMed
Kobatake, E. & Tanaka, K. (1991). Selective neuronal responses to complex visual object-features are already present in posterior part of the macaque inferotemporal cortex. Society for Neuroscience Abstracts 17, 443.Google Scholar
Kobatake, E. & Tanaka, K. (1992). Selectivity for features beyond orientation, color, size, and simple texture in the prestriate areas V2 and V4. Society for Neuroscience Abstracts 18, 146.Google Scholar
Kosslyn, S.M., Alpert, N.M., Thompson, W.L., Maljkovic, V., Weise, S.B., Chabris, C.F., Hamilton, S.E., Rauch, S.L. & Buonanno, F.S. (1993). Visual mental imagery activates topographically organized visual cortex: PET Investigations. Journal of Cognitive Neuroscience 5, 263–287.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1989). Cortical integration of parallel pathways in the visual system of primates. Brain Research 478, 161–165.CrossRefGoogle ScholarPubMed
Lachica, E.A., Mavity-Hudson, J.A. & Casagrande, V.A. (1991). Morphological details of primate axons and dendrites revealed by extracellular injection of biocytin: An economic and reliable alternative to PHA-L. Brain Research 564, 1–11.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Lund, J.S., Hendrickson, A.E., Ogren, M.P. & Tobin, E.A. (1981). Anatomical organization of primate visual cortex area VII. Journal of Comparative Neurology 202, 19–45.CrossRefGoogle ScholarPubMed
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1988). An investigation of collateral projections of the dorsal lateral geniculate nucleus and other subcortical structures to cortical areas V1 and V4 in the macaque monkey: A double-label retrograde tracer study. Experimental Brain Research 69, 651–661.CrossRefGoogle ScholarPubMed
Maguire, W.M. & Baizer, J.S. (1984). Visuotopic organization of the prelunate gyrus in rhesus monkey. Journal of Neuroscience 4, 1690–1704.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
Mignard, M. & Malpeli, J.G. (1991). Paths of information flow through visual cortex. Science 251, 1249–1251.CrossRefGoogle ScholarPubMed
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555–578.CrossRefGoogle ScholarPubMed
Mumford, D. (1992). On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biological Cybernetics 66, 135–145.CrossRefGoogle ScholarPubMed
Nakamura, H., Gattass, R., Desimone, R. & Ungerleider, L.G. (1993). The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. Journal of Neuroscience 13, 3681–3691.CrossRefGoogle ScholarPubMed
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
Rockland, K.S. (1989). Bistratified distribution of individual axons projecting from area V1 to MT in the macaque. Visual Neuroscience 3, 155–170.CrossRefGoogle Scholar
Rockland, K.S. (1992). Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey. Cerebral Cortex 2, 353–374.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1994). The organization of feedback connections from area V2 (18) to V1 (17). In Cerebral Cortex, Vol. 10, ed. Peters, A. & Rockland, K.S., pp. 261–299. New York: Plenum Press.Google Scholar
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, 3–20.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Virga, A. (1989). Terminal arbors of individual “feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported. Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology 285, 54–72.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Virga, A. (1990). Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey. Visual Neuroscience 4, 11–28.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Van Hoesen, G.W. (1994). Direct temporal-occipital feedback connections to striate cortex (VI) in the macaque monkey. Cerebral Cortex 4 (in press).CrossRefGoogle Scholar
Rosa, M.G.P., Soares, J.G.M., Fiorani, M. & Gattass, R. (1993). Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and Old World monkeys. Visual Neuroscience 10, 827–855.CrossRefGoogle ScholarPubMed
Saleem, K.S., Tanaka, K. & Rockland, K.S. (1993 a). Organization of afferent connections from the prestriate area V4 to the posterior part of the inferotemporal cortex in the macaque monkey. AR VO Abstract 4.Google Scholar
Saleem, K.S., Tanaka, K. & Rockland, K.S. (1993 b). Specific and columnar projections from area TEO to TE in the macaque inferotemporal cortex. Cerebral Cortex 3, 454–464.CrossRefGoogle ScholarPubMed
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons in the macaque. Journal of Neuroscience 10, 3369–3389.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1993). The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey. Visual Neuroscience 10, 717–746.CrossRefGoogle ScholarPubMed
Shjpp, S. & Zeki, S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–325.Google Scholar
Shtpp, S. & Zeki, S. (1989 a). The organization of connections between areas V5 and V1 in macaque monkey visual cortex. European Journal of Neuroscience 1, 309–332.Google Scholar
Shipp, S. & Zeki, S. (1989 b). The organization of connections between areas V5 and V2 in macaque monkey visual cortex. European Journal of Neuroscience 1, 333–354.CrossRefGoogle ScholarPubMed
Sousa, A.P.B., Piñon, M.C.G.P., Gattass, R. & Rosa, M.G.P. (1991). Topographic organization of cortical input to striate cortex in the cebus monkey: A fluorescent tracer study. Journal of Comparative Neurology 308, 665–682.CrossRefGoogle ScholarPubMed
Steele, G.E., Weller, R.E. & Cusick, C.G. (1991). Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys. Journal of Comparative Neurology 306, 495–520.CrossRefGoogle ScholarPubMed
Steele, G.E. & Weller, R.E. (1992). Arborization patterns of individual axons projecting from caudal to rostral inferior temporal cortex in squirrel monkeys. Society for Neuroscience Abstracts 18, 294.Google Scholar
Tanaka, K., Saito, H., Fukuda, Y. & Moriya, M. (1991). Coding visual images of objects in the inferotemporal cortex of the macaque monkey. Journal of Neurophysiology 66, 170–189.CrossRefGoogle ScholarPubMed
Tanaka, M., Lindsley, E., Lausmann, S. & Creutzfeldt, O.D. (1990). Afferent connections of the prelunate visual association cortex (areas V4 and DP). Anatomy and Embryology 181, 19–30.CrossRefGoogle ScholarPubMed
Tigces, J., Tigges, M., Anschel, S., Cross, N.A., Letbetter, W.D. & McBride, R.L. (1981). Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19 and MT in the squirrel monkey (Saimiri). Journal of Comparative Neurology 202, 539–560.CrossRefGoogle Scholar
Tononi, G., Sporns, O. & Edelman, G.M. (1992). Reentry and the problem of integrating multiple cortical areas: Simulation of dynamic integration in the visual system. Cerebral Cortex 2, 310–335.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkbj, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549–586. Cambridge: MIT Press.Google Scholar
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Walsh, V., Butler, S.R., Carden, D. & Kulikowski, J.J. (1992). The effects of V4 lesions on the visual abilities of macaques: Shape discrimination. Behavioural Brain Research 50, 115–126.CrossRefGoogle ScholarPubMed
Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1993). Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. Journal of Comparative Neurology 335, 73–91.CrossRefGoogle ScholarPubMed
Weller, R.E. & Steele, G.E. (1992). Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Journal of Comparative Neurology 324, 37–66.CrossRefGoogle ScholarPubMed
Yaginuma, S., Osawa, Y., Yamaguchi, K. & Iwai, E. (1993). Differential functions of central and peripheral visual field representations in monkey prestriate cortex. In Brain Mechanisms of Perception and Memory, ed. Ono, T., Squire, L.R., Raichle, M.E., Perrett, D.I. & Fukada, M., pp. 3–15. Oxford: Oxford University Press.Google Scholar
Yoshioka, T., Levitt, J.B. & Lund, J.S. (1992). Intrinsic lattice connections of macaque monkey visual cortical area V4. Journal of Neuroscience 12, 2785–2802.CrossRefGoogle ScholarPubMed
Zeki, S.M. & Shipp, S. (1989). Modular connections between areas V2 and V4 of macaque monkey visual cortex. European Journal of Neuroscience 1, 494–506.CrossRefGoogle ScholarPubMed