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The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques
Open accessAbstract
In addition to the major anatomical pathways from V1 into the temporal lobe, there are other smaller, “bypass” routes that are poorly understood. To investigate the direct projection from V1 to V4 (bypassing V2) and from V2 to TEO (bypassing V4), we injected the foveal and parafoveal representations of V4 and TEO with different retrograde tracers in five hemispheres of four macaques and analyzed the distributions of labeled neurons in V1 and V2 using flattened preparations of the cortex. In V1, labeled neurons were seen after injections in V4 but not TEO. The V4-projecting neurons were located in the foveal representation of V1, in both cytochrome oxidase (CO)-rich blobs and CO-poor interblob regions. In V2, TEO-projecting neurons were intermingled with V4-projecting neurons, although the former were far sparser than the latter. Across the cases, 6–19% of the TEO-projecting neurons were double labeled, that is, also projected to area V4. Both V4- and TEO-projecting neurons formed bands that ran orthogonal to the V1/V2 border, and both were located in CO-rich thin stripes and CO-poor interstripe regions. In some cases, a continuous band of V4-projecting neurons was also found along the V1/V2 border in the foveal representation of V2. The results indicate that the pathways from V1 to V4 and from V2 to TEO involve anatomical subcompartments thought to be concerned with both color and form. These “bypass” routes may allow coarse information about color and form to arrive rapidly in the temporal lobe. The bypass route from V2 to TEO might explain the partial sparing of color and form vision that is seen after lesions of V4. By analogy, given the bypass route from the foveal representation of V1 to V4, lesions of V2 affecting the foveal visual field would also be insufficient to block color and form vision.
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“In addition to the main routes through the V4 to the IT cortex (4), the model also accounts for the bypass routes (38) from V2 to the posterior inferotemporal cortex and from V4 to the anterior inferotemporal cortex (Fig. 1) [unlike the original model (5)].”
From A feedforward architecture accounts for rapid categorization (2007) · cites this paper as [38]
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InfluentialSelf-citationDivergent feedback connections from areas V4 and TEO in the macaque
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Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey
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“…was true for all the images examined.the only region of V4 that receives direct input from V1 Because V2 and foveal V4 display organization for both(Nakamura et al. 1993; Yukie and Iwai 1985) and, unlike the surround suppression and orientation, one natural issue isregions of V4 that represent…”
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“The cortical locus (prelunate gyrus) located between LS and STS and 35 mm lateral from the midline was selected as a representative area of V4 in macaques for both optical imaging and single-cell recordings (Shipp and Zeki, 1985; Desimone and Schein, 1987; Gattass et al., 1988; Schiller and Lee, 1991; Gallant et al.,…”
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“The output from them is channelled to area V4 through layers 2 and 3 of V1, both directly and through another subcompartment of area V2 (Zeki and Shipp, 1989; Nakamura et al., 1993) (Fig.”
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“…beyond V1 and V2 receive input from different and specialised compartments of V1, either directly or through specialised compartments of V2, as well as from other sites (see below) (Livingstone and Hubel 1984, Shipp and Zeki 1989a, Shipp and Zeki 1989b, Zeki and Shipp 1989, Nakamura et al. 1993).”
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“There is no obvious alternation in the density of connections between interstripes and area V4 (Zeki & Shipp, 1989b; Nakamura et al., 1993; DeYoe et al., 1994; Munk et al., 1995; Felleman et al., 1997), and neither does any interstripe connect to V5 (unlike thick stripes) (Shipp & Zeki, 1989 b).”
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“The projections revealed by these axonal tracing data are complex and not strictly sequential, including bypass connections such as those from V1 to V4 bypassing V2 (Nakamura et al. 1993).”
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“This area receives projections from V2 and is consistent with that portion of dorsal V4 termed the caudal dorsolateral visual complex (Shipp and Zeki, 1985; Nakamura et al., 1993; Stepniewska et al., 2005).”
BackgroundMethodA neural model of surface perception: Lightness, anchoring, and filling-in
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“This projection arises from V1 neurons in layer 2–3 (Yukie and Iwai, 1985; Nakamura et al., 1993).”
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What do we know about laminar connectivity?
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“However, as magnocellular projections might account for as much as half of the information in the ventral pathway (Ferrera et al., 1992; Nealey & Maunsell, 1994), such interactions could also take place within the ventral stream itself (Sherman, 1985; Nakamura et al., 1993).”
BackgroundObject vision and visual awareness
Logethetis, N. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80043-3 · Cited by 82
Segregation and convergence of specialised pathways in macaque monkey visual cortex.
Shipp, S. D., & Zeki, S. (1995) · Europe PMC (PubMed Central) · Cited by 81
Sutula, T. P., Zhang, P., Lynch, M., Sayın, Ü., Golarai, G., & Rod, R. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980126)390:4 · Cited by 118
Visual Functions of Primate Area V4
Pasupathy, A., Popovkina, D. V., & Kim, T. (2020) · Annual Review of Vision Science · doi:10.1146/annurev-vision-030320-041306 · Cited by 83
“While much of peripheral V4 receives feedforward projections primarily from V2, central representations receive projections from V1 that bypass V2 (Nakamura et al. 1993).”
BackgroundHow deep is the brain? The shallow brain hypothesis
Suzuki, M., Pennartz, C. M. A., & Aru, J. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00756-z · Cited by 79
“Electrophysiological evidence supported this view 35–37 , such as the presence of larger receptive fields and longer onset latencies in higher compared with intermediate or lower cortical areas.”
BackgroundShipp, S. D. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1363 · Cited by 78
“Charts from V2 are more comparable, in that all three areas connect to V2, whereas the connections of V4 with V1 are limited to the foveal region (Cragg, 1969; Zeki, 1969; Yukie and Iwai, 1985; Nakamura et al., 1993).”
BackgroundNapieralski, J. A., Butler, A., & Chesselet, M. ‐. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960930)373:4 · Cited by 131
The functional neuroanatomy of face perception: from brain measurements to deep neural networks
Kalanit Grill-spector, A., Weiner, K. S., Gomez, J., Anthony Stigliani, A., & Natu, V. S. (2018) · Interface Focus · doi:10.1098/rsfs.2018.0013 · Cited by 82
Zeki, S., & Bartels, A. (1999) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1999.0485 · Cited by 73
“The reciprocal connections between these areas (Zeki and Shipp 1989, Nakamura et al. 1993, Rockland et al. 1994) make it equally likely that the operation is a cooperative one involving all these areas; this is especially so since, in monkey, the wavelength selective cells of V1 are indifferent to…”
BackgroundRosa, M. G. P., Palmer, S., Gamberini, M., Tweedale, R., Piñon, M. C., & Bourne, J. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20412 · Cited by 71
“In addition, this pattern is distinct from the ones observed after injections centered in V2 (Lund et al., 1975; Wong-Riley, 1978; Rockland and Pandya, 1979), V4 (Nakamura et al., 1993), and MT (Shipp and Zeki, 1989; Vogt-Weisenhorn et al., 1995).”
Inferior Parietal Lobule Projections to Anterior Inferotemporal Cortex (Area TE) in Macaque Monkey
Zhong, Y. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.5.527 · Cited by 71
Friedemann Pulvermüller, A., & Garagnani, M. (2014) · Cortex · doi:10.1016/j.cortex.2014.02.015 · Cited by 74
“1, Discussion) and in previous publications (Garagnani et al., 2008, 2009; Garagnani & Pulvermüller, 2011; Garagnani & Pulvermüller, 2013).”
Ferro, D., van Kempen, J., Boyd, M., Panzeri, S., & Thiele, A. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2022097118 · Cited by 75
“Direct projections from V1 to V4 are largely restricted to the central 6° of the visual field (64, 65).”
BackgroundCowell, R. A., Bussey, T. J., & Saksida, L. M. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21373 · Cited by 75
“In addition, there is evidence that “jumping” connections in the VVS are also abundant, for example, between area V1 and V3, bypassing area V2 (Lennie, 1998), from V2 to TEo ( Nakamura, Gattass, Desimone, & Ungerleider, 1993 ), and from V4 to posterior TE (Saleem, Tanaka, & Rockland, 1992).”
BackgroundStepniewska, I., Collins, C. E., & Kaas, J. H. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh182 · Cited by 67
“As central V4 has been described as having inputs from central V1 (Zeki, 1978; Nakamura et al., 1993), it was not surprising to find a few labeled neurons in V1 corresponding to central vision of the lower quadrant near the representation of the vertical meridian.”
InfluentialArea V4 in Cebus monkey: extent and visuotopic organization
Piñon, M. C. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.8.685 · Cited by 67
“…in Cebus, based on anatomical connections (Piñon et al., 1990; Sousa et al., 1991) and are also comparable with those of area V4 defined in Macaca based on electrophysiology (Gattass et al., 1988a) as well as on anatomical connections with area V2 (Nakamura et al., 1993; Gattass et al. , Figure 11.”
BackgroundResultALBERT-LUDWIGS-UNIVERSIT ¨ AT FREIBURG
Systeme, A. A. I., Burgard, W., & Domínguez, R. S. (2006) · Cited by 67
Architecture, Connectivity, and Transmitter Receptors of Human Extrastriate Visual Cortex
Zilles, K., & Clarke, S. (1997) · Cerebral cortex · doi:10.1007/978-1-4757-9625-4_15 · Cited by 66
Elements of Cortical Architecture
Rockland, K. S. (1997) · Cerebral cortex · doi:10.1007/978-1-4757-9625-4_6 · Cited by 67
Visual latencies in cytochrome oxidase bands of macaque area V2.
Munk, M. H. J., Nowak, L. G., Girard, P., Chounlamountri, N., & Bullier, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.4.988 · Cited by 64
Fryer, R. H., Kaplan, D. R., Feinstein, S. C., Radeke, M. J., Grayson, D. R., & Kromer, L. F. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961007)374:1 · Cited by 273
Temporal Limitations in Object Processing Across the Human Ventral Visual Pathway
McKeeff, T. J., Remus, D. A., & Tong, F. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00568.2006 · Cited by 61
Maniglia, M., Pavan, A., Cuturi, L. F., Campana, G., Sato, G., & Casco, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025568 · Cited by 57
“Cell recordings pointed out the existence of direct projections from V1 to V4 bypassing V2 [44].”
BackgroundNeural mechanisms of cortico–cortical interaction in texture boundary detection: a modeling approach
Thielscher, A., & Heiko Neumann, B. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.08.050 · Cited by 53
“Third, weak direct bi-directional connections between V1 and V4 have been regularly reported (Felleman and van Essen, 1991; Nakamura et al., 1993; Rockland et al., 1994; Zilles and Clarke, 1997).”
BackgroundThe Role of Visual Area V4 in the Discrimination of Partially Occluded Shapes
Kosai, Y., El-Shamayleh, Y., Fyall, A. M., & Pasupathy, A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1375-14.2014 · Cited by 55
Arcaro, M. J., Honey, C. J., Mruczek, R. E. B., Kästner, S., & Hasson, U. (2015) · eLife · doi:10.7554/elife.03952 · Cited by 53
“…a broader-scale anatomical organization of direct (and indirect) connections, facilitated via differences in intra-areal projections between cortical sites representing central and peripheral space (Colby et al., 1988; Nakamura et al., 1993; Gattass et al., 2005; Ungerleider et al., 2008, 2014).”
BackgroundArcaro, M. J., & Kästner, S. (2015) · Visual Neuroscience · doi:10.1017/s0952523815000115 · Cited by 49
“As revealed in monkey tracer studies, the fovea of V1, but not periphery, projects directly to V4 (Zeki, 1969 a ; Nakamura et al., 1993 ).”
BackgroundThe color selectivity of neurons in posterior inferior temporal cortex of macaque monkey
Yasuda, M., ヤスダ, マ., & YASUDA, M. (2007) · SOKENDAI (Graduate University for Advanced Studies) · Cited by 50
Visual perception and memory systems: from cortex to medial temporal lobe
Khan, Z. U., Martín‐Montañez, E., & Baxter, M. G. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0641-6 · Cited by 53
“extrastriate cortical areas and temporal areas downstream of V4, including temporal areas F (TF) and H (TH) and the various subdivisions of IT cortex [18–20].”
BackgroundGaragnani, M., & Friedemann Pulvermüller, A. (2013) · Brain and Language · doi:10.1016/j.bandl.2013.02.001 · Cited by 54
Barbur, J. L., Weiskrantz, L., & Harlow, J. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11637 · Cited by 46
Responses of Spectrally Selective Cells in Macaque Area V2 to Wavelengths and Colors
Moutoussis, K., & Zeki, S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00248.2001 · Cited by 43
“…et al. 1988; Ts’o and Gilbert 1988) and project mainly to V4 (DeYoe and Van Essen 1985; DeYoe et al. 1994; Felleman et al. 1997; Malach et al. 1994; Nakamura et al. 1993; Shipp and Zeki 1985; Xiao et al. 1999; Zeki and Shipp 1989), an area specialized in color processing (Zeki 1973, 1977,…”
Background
Metadata
- Authors
- Nakamura, H., Gattass, R., Desimone, R., & Ungerleider, L.
- Affiliations
- National Institute of Mental Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1993-09-01
- Volume
- 13
- Issue
- 9
- Pages
- 3681-3691
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6576450
- OpenAlex
- W1527855123
- Cited by
- 211
- References
- 82
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 5 · 2023: 7 · 2022: 4 · 2021: 4 · 2020: 5 · 2019: 5 · 2018: 5 · 2017: 7 · 2016: 4 · 2015: 8 · 2014: 10 · 2013: 3 · 2012: 4
- FWCI
- 4.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- visual cortex, area V1, V2, area V4, cortical projections, cytochrome oxidase blobs, color vision, form vision, retrograde tracing, macaque, foveal representation
- MeSH terms
- Amidines, Animals, Axonal Transport, Electron Transport Complex IV, Fluorescent Dyes, Horseradish Peroxidase, Macaca mulatta, Neurons, Occipital Lobe, Temporal Lobe, Visual Fields, Visual Pathways, Wheat Germ Agglutinins, Biomarkers, Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate
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