Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-09T23:04:31.142Z Has data issue: false hasContentIssue false
  • English
  • Français

Qualitative and quantitative features of axons projecting from caudal to rostral inferior temporal cortex of squirrel monkeys

Published online by Cambridge University Press:  02 June 2009

G.E. Steele  and
R.E. Weller
G.E. Steele
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
R.E. Weller
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
Get access Rights & Permissions [Opens in a new window]

Abstract

On the basis of cortical and subcortical connections and architectonics, inferior temporal (IT) cortex of squirrel monkeys consists of a caudal region, ITC, with dorsal (ITCd) and ventral (ITCv) subdivisions; a rostral region, ITR; and possibly a third region intermediate to ITC and ITR, IT1 (Weller & Steele, 1992; Steele & Weller, 1993). The present study qualitatively and quantitatively examined the terminal arborizations of 26 axons in ITR and IT1 labeled by injections of biocytin or, in one case, horseradish peroxidase, in ITCv. The majority of axons gave rise to a single terminal arbor, with a small number branching into two overlapping or nearby arbors. Presumptive terminal specializations consisted of rounded, bead-like swellings, most often located en passant. All axons terminated in layer 4 of cortex, and most had additional terminations in layers 3 and 5. The total extent of each axon's terminal arbor was 125–750 μm dorsoventrally (mean = 360.6 μm) and 150–725 μm anteroposteriorly (mean = 328.1 μm; all values uncorrected for shrinkage). In most axons, especially those with larger terminal fields, boutons were not uniformly distributed, but formed 2–4 clumps (mean = 2.2), with a mean width of 149 μm, separated by narrower regions of fewer boutons. Based on a cluster analysis of characteristics of the 26 axons, axons projecting from caudal (ITCv) to rostral (ITR or IT1) IT cortex of squirrel monkeys comprised three groups that we called Type I, Type II, and Type III. Type I axons, the smallest in areal extent of terminal arbor, terminated predominantly in dorsal ITR. Type III axons, largest in areal extent, and Type II axons, intermediate in areal extent, terminated in ventral ITR and throughout IT1. The three classes of axons may correspond to different types of visual information entering rostral IT cortex. The clumping of boutons suggests that individual axons terminate in limited patches within their terminal fields.

Keywords

Axon terminalsBiocytinVisual cortexPrimateModular organization
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 4 , July 1995 , pp. 701 - 722
Copyright
Copyright © Cambridge University Press 1995

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

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 6, 775.CrossRefGoogle Scholar
Amir, Y., Harel, M. & Malach, R. (1993). Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. Journal of Comparative Neurology 334, 19–46.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
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1985). Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Research 342, 91–102.CrossRefGoogle ScholarPubMed
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1987). Functional subdivisions of the temporal lobe neocortex. Journal of Neuroscience 7, 330–342.CrossRefGoogle ScholarPubMed
Baylis, G.C. & Rolls, E.T. (1987). Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks. Experimental Brain Research 65, 614–622.CrossRefGoogle ScholarPubMed
Blake, L., Jarvis, C.D. & Mishkin, M. (1977). Pattern discrimination thresholds after partial inferior temporal or lateral striate lesions in monkeys. Brain Research 120, 209–220.CrossRefGoogle ScholarPubMed
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. & Ungerleider, L.G. (1991). Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554–575.CrossRefGoogle ScholarPubMed
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychophysical performance. Journal of Neuroscience 12, 4745–4765.CrossRefGoogle Scholar
Brown, M.W., Wilson, F.A.W. & Riches, I.P. (1987). Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory. Brain Research 409, 158–162.CrossRefGoogle ScholarPubMed
Bugbee, N.M. & Goldman-Rakic, P.S. (1983). Columnar organization of corticocortical projections in squirrel and rhesus monkeys: Similarity of column width in species differing in cortical volume. Journal of Comparative Neurology 220, 355–364.CrossRefGoogle ScholarPubMed
Chelazzi, L., Miller, E.K., Duncan, J. & Desimone, R. (1993). A neural basis for visual search in inferior temporal cortex. Nature 363, 345–347.CrossRefGoogle ScholarPubMed
Cirillo, R.A., George, P.J., Horel, J.A. & Martin-Elkins, C. (1989). An experimental test of the theory that visual information is stored in the inferotemporal cortex. Behavioural Brain Research 34, 43–53.CrossRefGoogle ScholarPubMed
Costello, R.K., Dickinson, C., Rosenberger, A.L., Boinski, S. & Szalay, F.S. (1993). Squirrel monkey (genus Saimiri) taxonomy: A multidisciplinary study of the biology of species. In Species, Species Concepts, and Primate Evolution, ed. Kimbel, W.H. & Martin, L.B., pp. 177–210. New York: Plenum Press.CrossRefGoogle Scholar
Cowey, A. & Gross, C.G. (1970). Effects of foveal prestriate and inferotemporal lesions on visual discrimination by rhesus monkeys. Experimental Brain Research 11, 128–144.CrossRefGoogle ScholarPubMed
Dean, P. (1982). Visual behavior in monkeys with inferotemporal lesions. In Advances in the Analysis of Visual Behavior, ed. Ingle, D.J., Mansfield, R.J., & Goodale, M.S., pp. 587–628. Cambridge, MA: MIT Press.Google Scholar
Desimone, R. (1992). The physiology of memory: Recordings of things past. Science 258, 245–246.CrossRefGoogle ScholarPubMed
Desimone, R., Albright, T.D., Gross, C.G. & Bruce, C. (1984). Stimulus selective properties of inferior temporal neurons in the macaque. Journal of Neuroscience 4, 2051–2062.CrossRefGoogle ScholarPubMed
Desimone, R., Fleming, J. & Gross, C.G. (1980). Prestriate afferents to inferior temporal cortex: An HRP study. Brain Research 184, 41–55.CrossRefGoogle ScholarPubMed
Desimone, R. & Gross, C.G. (1979). Visual areas in the temporal cortex of the macaque. Brain Research 178, 363–380.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual processing in monkeys. In Handbook of Neuropsychology Vol. 2, ed. Boller, F. & Grafman, J., pp. 267–299. New York: Elsevier.Google Scholar
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in primate cerebral cortex. Cerebral Cortex 1, 1–47.CrossRefGoogle ScholarPubMed
Florence, S.L. & Casagrande, V. (1987). Organization of individual afferent axons in layer IV of striate cortex in a primate. Journal of Neuroscience 7, 3850–3868.CrossRefGoogle ScholarPubMed
Florence, S.L. & Casagrande, V. (1990). Development of geniculocortical axon arbors in a primate. Visual Neuroscience 5, 291–309.CrossRefGoogle ScholarPubMed
Florence, S.L. & Kaas, J.H. (1992). Ocular dominance columns in area 17 of Old World macaque and talapoin monkeys: Complete reconstructions and quantitative analyses. Visual Neuroscience 8, 449–462.CrossRefGoogle ScholarPubMed
Fujita, I. & Fujita, T. (1993). Intrinsic connections in the macaque inferotemporal cortex: Anatomical substrate for functional columns. Society for Neuroscience Abstracts 19, 971.Google Scholar
Fujita, I., Tanaka, K., Ito, M. & Cheng, K. (1992). Columns for visual features of objects in monkey inferotemporal cortex. Nature 360, 343–346.CrossRefGoogle ScholarPubMed
Fuster, J.M. & Jervey, J.P. (1981). Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. Science 212, 952–955.CrossRefGoogle ScholarPubMed
Gattass, R., Rosa, M.G.P., Sousa, A.P.B., Pinon, M.C.G., Fiorani, M. Jr., & Neuenschwander, S. (1990). Cortical streams of visual information processing in primates. Brazilian Journal of Medical and Biological Research 23, 375–393.Google ScholarPubMed
Gochin, P.M., Miller, E., Gross, C.G. & Gerstein, G. (1991). Functional interactions among neurons in inferior temporal cortex of the awake macaque. Experimental Brain Research 84, 505–516.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P.S. & Schwartz, M.L. (1982). Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Science 216, 755–757.CrossRefGoogle ScholarPubMed
Gross, C.G. (1973). Visual functions of inferotemporal cortex. In Handbook of Sensory Physiology, ed. Jung, R., pp. 451–482. Berlin, Germany: Springer-Verlag.Google Scholar
Gross, C.G., Bender, D.B. & Gerstein, G.L. (1979). Activity of inferior temporal neurons in behaving monkeys. Neuropsychologia 17, 215–229.CrossRefGoogle ScholarPubMed
Gross, C.G., Cowey, A. & Manning, F.J. (1971). Further analysis of visual discrimination deficits following foveal prestriate and inferotemporal lesions in rhesus monkeys. Journal of Comparative and Physiological Psychology 76, 1–7.CrossRefGoogle ScholarPubMed
Gross, C.G. & Mishkin, M. (1977). The neural basis of stimulus equivalence across retinal translation. In Lateralization in the Nervous System, ed. Harnad, S., Doty, R., Jaynes, J., Goldstein, L. & Krauthamer, G., pp. 109–122. New York: Academic Press.CrossRefGoogle Scholar
Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. (1972). Visual properties of neurons in inferotemporal cortex of the macaque. Journal of Neurophysiology 35, 96–111.CrossRefGoogle ScholarPubMed
Gross, C.G., Rodman, H.R., Gochin, P.M. & Colombo, M.W. (1993). Inferior temporal cortex as a pattern recognition device. In Computational Learning and Cognition: Proceedings of the 3rd NEC Research Symposium, ed. Baum, E., pp. 44–73. Philadelphia, PA: Siam.Google Scholar
Horel, J.A. (1984). Cold lesions in inferotemporal cortex produce reversible deficits in learning and retention of visual discriminations. Physiological Psychology 12, 259–270.CrossRefGoogle Scholar
Horel, J.A., Pytko-Joiner, D.E., Voytko, M.L. & Salsbury, K. (1987). The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behavioral Brain Research 23, 29–42.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1977). Functional architecture of macaque monkey visual cortex. Proceedings of the Royal Society B (London) 198, 1–59.Google ScholarPubMed
Iwai, E. & Mishkin, M. (1968). Two visual foci in the temporal lobe of monkeys. In Neuropsychological Bases of Learning and Behavior, ed. Yoshii, N. & Buchwald, N.A., pp. 1–8. Japan: Osaka University Press.Google Scholar
Iwai, E. & Mishkin, M. (1969). Further evidence on the locus of the visual area in the temporal lobe of the monkey. Experimental Neurology 25, 585–594.CrossRefGoogle ScholarPubMed
Iwai, E., Yukie, M., Suyama, H. & Shirakawa, S. (1987). Amygdalar connections with middle and inferior temporal gyri of the monkey. Neuroscience Letters 83, 25–29.CrossRefGoogle ScholarPubMed
Izzo, P. (1991). A note on the use of biocytin in anterograde tracing studies in the central nervous system: Application at both light and electron microscopic level. Journal of Neuroscience Methods 36, 155–166.CrossRefGoogle ScholarPubMed
Kobatake, E. & Tanaka, K. (1994). Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. Journal of Neurophysiology 71, 856–867.CrossRefGoogle ScholarPubMed
Komatsu, H. & Ideura, Y. (1993). Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the monkey. Journal of Neurophysiology 70, 677–694.CrossRefGoogle ScholarPubMed
Komatsu, H., Ideura, Y., Kaji, S. & Yamane, S. (1992). Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey. Journal of Neuroscience 12, 408–424.CrossRefGoogle ScholarPubMed
Krubitzer, L.A., Calford, M.B. & Schmid, L.M. (1993). Connections of somatosensory cortex in megachiropteran bats: The evolution of cortical fields in mammals. Journal of Comparative Neurology 327, 473–506.CrossRefGoogle ScholarPubMed
Kuypers, H.G., Szwarcbart, M.K., Mishkin, M. & Rosvold, H.E. (1965). Occipitotemporal corticocortical connections in the rhesus monkey. Experimental Neurology 11, 245–262.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1993). The morphology of collicular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus. Visual Neuroscience 10, 403–418.CrossRefGoogle ScholarPubMed
Lachica, E.A., Mavity-Hudson, J.A. & Casagrande, V.A. (1991). Morphological details of primate axons and dendrites revealed by extracellular injections of biocytin: An economic and reliable alternative to PHA-L. Brain Research 564, 1–11.CrossRefGoogle ScholarPubMed
LeVay, S. (1988). Patchy intrinsic projections in visual cortex, area 18, of the cat: Morphological and immunocytochemical evidence for an excitatory function. Journal of Comparative Neurology 269, 265–274.CrossRefGoogle ScholarPubMed
LeVay, S. & Nelson, S.B. (1991). Columnar organization of the visual cortex. In The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 266–315. Boca Raton, Florida: CRC Press.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Lorente de Nó, R. (1949). Cerebral cortex: Architecture, intracortical connections, motor projections. In Physiology of the Nervous System, ed. Fulton, J.F., pp. 288–312. London: Oxford University Press.Google Scholar
Lueschow, A., Miller, E.K. & Desimone, R. (1994). Inferior temporal mechanisms for invariant object recognition. Cerebral Cortex 5, 523–531.CrossRefGoogle Scholar
Lund, J.S., Yoshioka, T. & Levitt, J.B. (1993). Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cerebral Cortex 3, 148–162.CrossRefGoogle ScholarPubMed
Malach, R., Amir, Y., Harel, M. & Grinvald, A. (1993). Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 90, 10469–10473.CrossRefGoogle ScholarPubMed
Martin-Elkins, C.L. & Horel, J.A. (1992). Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA-HRP. Journal of Comparative Neurology 321, 177–192.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
Maxwell, A.E. (1977). Multivariate Analysis in Behavioural Research. New York: John Wiley and Sons.Google Scholar
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369–402.CrossRefGoogle ScholarPubMed
Miller, E.K. & Desimone, R. (1994). Parallel neuronal mechanisms for short-term memory. Science 263, 520–522.CrossRefGoogle ScholarPubMed
Miller, E.K., Gochin, P.M. & Gross, C.G. (1991). Habituation-like decrease in the responses of neurons in inferior temporal cortex of the macaque. Visual Neuroscience 7, 357–362.CrossRefGoogle ScholarPubMed
Miller, E.K., Li, L. & Desimone, R. (1993). Activity of neurons in anterior inferior temporal cortex during a short-term memory task. Journal of Neuroscience 13, 1460–1478.CrossRefGoogle ScholarPubMed
Mishkin, M. (1982). A memory system in the monkey. Philosophical Transactions of the Royal Society B (London) 298, 85–95.Google ScholarPubMed
Miyashita, Y. (1988). Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335, 817–820.CrossRefGoogle ScholarPubMed
Miyashita, Y. (1993). Inferior temporal cortex: Where visual perception meets memory. Annual Review of Neuroscience 16, 245–263.CrossRefGoogle ScholarPubMed
Miyashita, Y. & Chang, H.S. (1988). Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 68–70.CrossRefGoogle ScholarPubMed
Miyashita, Y., Date, A. & Okuno, H. (1993). Configurational encoding of complex visual forms by single neurons of monkey temporal cortex. Neuropsychologia 31, 1119–1131.CrossRefGoogle ScholarPubMed
Moran, J. & Desimone, R. (1985). Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784.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
Mountcastle, V.B. (1957). Modality and topographic properties of single neurones of cat's somatic sensory cortex. Journal of Neurophysiology 20, 408–434.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
Norita, M., McHaffie, J.G., Shimizu, H. & Stein, B.E. (1991). The corticostriatal and corticotectal projections of the feline lateral suprasylvian cortex demonstrated with anterograde biocytin and retrograde fluorescent techniques. Neuroscience Research 10, 149–155.CrossRefGoogle ScholarPubMed
Norusis, M.J. (1986 a). SPSS/PC+. Chicago, Illinois: SPSS Inc.Google Scholar
Norusis, M.J. (1986 b). SPSS/PC+ Advanced Statistics. Chicago, Illinois: SPSS Inc.Google Scholar
Riches, I.P., Wilson, F.A.W. & Brown, M.W. (1991). The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate. Journal of Neuroscience 11, 1763–1779.CrossRefGoogle ScholarPubMed
Richmond, B.J. & Sato, T. (1987). Enhancement of inferior temporal neurons during visual discrimination. Journal of Neurophysiology 58, 1292–1306.CrossRefGoogle ScholarPubMed
Richmond, B.J., Wurtz, R.H. & Sato, T. (1983). Visual responses of inferior temporal neurons in awake rhesus monkey. Journal of Neurophysiology 50, 1415–1432.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1989). Bistratified distribution of terminal arbors of individual axons projecting from VI to MT in the macaque monkey. Visual Neuroscience 3, 155–170.CrossRefGoogle Scholar
Rockland, K.S. (1992). Laminar distribution of neurons projecting from area V1 to V2 in macaque and squirrel monkeys. Cerebral Cortex 2, 38–47.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Lund, J.S. (1983). Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 306–318.Google ScholarPubMed
Rockland, K.S., Lund, J.S., & Humphrey, A.L. (1982). Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). Journal of Comparative Neurology 209, 41–58.CrossRefGoogle 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
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and transspecies comparisons. Brain, Behavior, and Evolution 23, 121–164.Google ScholarPubMed
Sakai, K. & Miyashita, Y. (1991). Neural organization for the longterm memory of paired associates. Nature 354, 152–155.CrossRefGoogle ScholarPubMed
Saleem, K.S., Tanaka, K. & Rockland, K.S. (1992). PHA-L study of connections from TEO and V4 to TE in the monkey visual cortex. Society for Neuroscience Abstracts 18, 294.Google Scholar
Saleem, K.S., Tanaka, K. & Rockland, K.S. (1993 a). Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. Cerebral Cortex 3, 454–464.CrossRefGoogle ScholarPubMed
Saleem, K.S., Tanaka, K. & Rockland, K.S. (1993 b). Organization of afferent connections from the prestriate area V4 to the posterior part of the inferotemporal cortex in the macaque monkey. ARVO Abstracts 34, 1174.Google Scholar
Sáry, G., Vogels, R. & Orban, G.A. (1993). Cue-invariant shape selectivity of macaque inferior temporal neurons. Science 260, 995–997.CrossRefGoogle ScholarPubMed
Sato, T. (1988). Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque. Journal of Neurophysiology 60, 344–364.CrossRefGoogle ScholarPubMed
Sato, T. & Kawamura, T. (1990). Distribution of cells in area TE selectively responsive to visual patterns or color spots during matching two visual stimuli at different locations. Japanese Journal of Physiology 40, s238.Google Scholar
Schwartz, E.L., Desimone, R., Albright, T.D. & Gross, C.G. (1983). Shape recognition and inferior temporal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 80, 5776–5778.CrossRefGoogle ScholarPubMed
Sholl, D.A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. Journal of Anatomy 87, 387–406.Google 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
Steele, G.E. & Weller, R.E. (1993). Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Visual Neuroscience 10, 563–583.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
Tabachnik, B.G. & Fidell, L.S. (1989). Using Multivariate Statistics. New York: Harper and Row.Google Scholar
Tanaka, K. (1993). Neuronal mechanisms of object recognition. Science 262, 685–688.CrossRefGoogle ScholarPubMed
Tanaka, K., Saito, H.A., Fukada, 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
Tigges, J., Spatz, W.B. & Tigges, M. (1973). Reciprocal point-to-point connections between parastriate and striate cortex in the squirrel monkey (Saimiri). Journal of Comparative Neurology 148, 481–490.CrossRefGoogle ScholarPubMed
Tigges, J., Spatz, W.B. & Tigges, M. (1974). Efferent cortico-cortical fiber connections of area 18 in the squirrel monkey (Saimiri). Journal of Comparative Neurology 158, 219–236.CrossRefGoogle ScholarPubMed
Tigges, 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 squirrel monkey (Saimiri). Journal of Comparative Neurology 202, 539–560.CrossRefGoogle ScholarPubMed
Tootell, R.B.H. & Silverman, M.S. (1985). Two methods for flatmounting cortical tissue. Journal of Neuroscience Methods 15, 177–190.CrossRefGoogle ScholarPubMed
Turner, B.H., Mishkin, M. & Knapp, M. (1980). Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. Journal of Comparative Neurology 191, 515–543.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Advances in the Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549–586. Cambridge, Massachusetts: MIT Press.Google Scholar
Van Essen, D.C., Felleman, D.J., DeYoe, E.A., Olavarria, J. & Knierrim, J. (1990). Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. Cold Spring Harbor Symposia on Quantitative Biology 55, 679–698.CrossRefGoogle ScholarPubMed
Von Bonin, G. & Bailey, P. (1947). The Neocortex of Macaca mulatta. Urbana, Illinois: University of Illinois Press.Google Scholar
Webster, M.J., Ungerleider, L.G. & Bachevalier, J. (1991). Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. Journal of Neuroscience 11, 1095–1116.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1987). Subdivisions and connections of inferior temporal cortex in owl monkeys. Journal of Comparative Neurology 256, 137–172.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. (1990). Functional subdivisions of area TE of the inferotemporal cortex in the monkey. In Vision, Memory, and the Temporal Lobe, ed. Iwai, E. & Mishkin, M., pp. 29–41. New York: Elsevier.Google Scholar
Yukie, M., Takeuchi, H., Hasegawa, Y. & Iwai, E. (1990). Differential connectivity of inferotemporal area TE with the amygdala and the hippocampus in the monkey. In Vision, Memory and the Temporal Lobe, ed. Iwai, E. & Mishkin, M., pp. 129–135. New York: Elsevier.Google Scholar