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The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques
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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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Modularity in philosophy, the neurosciences, and psychiatry
Zielasek, J., & Gäebel, W. (2008) · Poiesis & Praxis · doi:10.1007/s10202-008-0065-z · Cited by 3
“…movements, i.e. the motor system (Gentner and Claasen 2006), clustered areas of brain activation in the medial part of the frontal lobe in empathy studies (Seitz et al. 2006), or information processing in the visual system (Nakamura et al. 1993, 2004; Felleman et al. 1997; Magen and Cohen 2007).”
BackgroundVisual Corticocortical Inputs to Ferret Area 18
Khalil, R., Louis, M. R. J. S., Alsuwaidi, S., & Levitt, J. B. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.581478 · Cited by 2
“, 1981; Kennedy and Bullier, 1985), V4 (or prelunate gyrus) (Rockland and Pandya, 1979; Kennedy and Bullier, 1985; Nakamura et al., 1993; Nascimento-Silva et al., 2014), V5/MT (or superior temporal sulcus) (Maunsell and Van Essen, 1983; Kennedy and Bullier, 1985; Ungerleider and Desimone, 1986; Rockland and Knutson, 2…”
BackgroundCortical field maps across human sensory cortex
Brewer, A. A., & Barton, B. (2023) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2023.1232005 · Cited by 4
“In comparison, the homologous regions in macaque monkey are relatively much smaller, comprising such areas as TEO and V4 (Desimone and Schein, 1987; Gattass et al., 1988; Boussaoud et al., 1991; Tanaka et al., 1991; Nakamura et al., 1993; Brewer et al., 2002).”
BackgroundTopographic organization across foveal visual areas in macaques
Li, H., Hu, D., Tanigawa, H., & Takahata, T. (2024) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1389067 · Cited by 2
Attention to distinguishing features in object recognition: An interactive-iterative framework
Baruch, O., Kimchi, R., & Goldsmith, M. (2017) · Cognition · doi:10.1016/j.cognition.2017.10.007 · Cited by 3
Naturally Computed Scale Invariance in the Residual Stream of ResNet18
Longon, A. (2025) · IEEE/CVF Conference on Computer Vision and Pattern Recognition Workshops (CVPRW) · doi:10.1109/cvprw67362.2025.00467 · Cited by 1
“Furthermore, this work suggests a function for so-called “bypass connections” in biological visual systems (macaque [13] and mouse [4]), an anatomical analogue to the residual stream.”
Pulvinar Structure, Circuitry & Function in Primates☆
Shipp, S. D. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04740-1 · Cited by 1
The Asynchrony of Visual Perception
(2004) · Elsevier eBooks · doi:10.1016/b978-012264841-0/50013-5 · Cited by 1
Lesions in primate visual cortex leading to deficits of visual perception
Merigan, W. H., & Pasternak, T. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198505822.003.0005 · Cited by 1
A computer model of the Land Mondrian retinex experiment
Romaya, J. P. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00905-2.x · Cited by 1
O posicionamento dos tribunais perante os contratos de distribuição (1980-2000)
Forgioni, P. A. (2005) · Americanae (AECID Library) · Cited by 1
Simulating semantic dementia in a brain-constrained model of action and object words learningPreprint
Efremov, A., Kuptsova, A., Wennekers, T., Юрьевич, Ш. Ю., Gutkin, B. S., & Garagnani, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.03.482066 · Cited by 1
“AT (44, 45).”
Functional architecture for speed tuning in primary visual cortex of carnivoresPreprint
Casanova, V. M. S., Lasky-Nielson, N., Ye, L., Touboul, J., Ribot, J., & Hooser, S. D. V. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.04.686504 · Cited by 1
“…projection patterns to extrastriate areas that resemble the projections to the thick and thin stripes of V2 in the primate (Livingstone and Hubel, 1984, 1987, 1988; DeYoe and Van Essan, 1985; Shipp and Zeik 1985, 1989; Felleman and Van Essen, 1991; Nakamura et al., 1993; Sincich and Horton, 2005).”
Exploration of the inter-areal cortico-cortical network of the macaque monkey
Markov, N. T. (2010) · theses.fr (ABES) · doi:10.70675/a52a5bb2zbe03z4b35za32dz74a333a8583f
Mechanisms of Object Representation in Inferotemporal Cortex
Rollenhagen, J. E. (2004) · D-Scholarship@Pitt (University of Pittsburgh)
Feature-based attention in primate visual cortex
Schwedhelm, P. (2016) · doi:10.53846/goediss-5732
Computational and Functional Specialization of Memory
Cowell, R., Bussey, T. J., & Saksida, L. M. (2016) · Wiley eBooks · doi:10.1002/9781118650813.ch11
Functional-Specific Projections from V2 to V4 in Macaque MonkeysPreprint
Chen, F., Yan, K., Liang, C., Wang, J., Cai, X., Zhang, R., & Lu, H. D. (2021) · Research Square · doi:10.21203/rs.3.rs-325966/v1
Redgrave, P. (2010) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.6172956.6215060
Hue and orientation pinwheels in macaque area V4
Parajuli, A., & Felleman, D. J. (2024) · Journal of Neurophysiology · doi:10.1152/jn.00366.2023
Comparative retinotopic mapping in macaques and humans
Vanduffel, W., & Zhu, Q. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-820480-1.00199-6
Projection-specific and reversible functional blockage in the association cortex of macaque monkeys
Yokoo, S., Higo, T., Gérard-Mercier, F., Oguchi, M., Sakagami, M., Bito, H., Sakamoto, M., Ichinohe, N., & Tanaka, K. (2025) · Neuroscience Research · doi:10.1016/j.neures.2025.05.004
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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