Segregation of feedforward and feedback projections in mouse visual cortex
Open accessAbstract
Hierarchical organization is a common feature of mammalian neocortex. Neurons that send their axons from lower to higher areas of the hierarchy are referred to as “feedforward” (FF) neurons, whereas those projecting in the opposite direction are called “feedback” (FB) neurons. Anatomical, functional, and theoretical studies suggest that these different classes of projections play fundamentally different roles in perception. In primates, laminar differences in projection patterns often distinguish the two projection streams. In rodents, however, these differences are less clear, despite an established hierarchy of visual areas. Thus the rodent provides a strong test of the hypothesis that FF and FB neurons form distinct populations. We tested this hypothesis by injecting retrograde tracers into two different hierarchical levels of mouse visual cortex (area 17 and anterolateral area [AL]) and then determining the relative proportions of double‐labeled FF and FB neurons in an area intermediate to them (lateromedial area [LM]). Despite finding singly labeled neurons densely intermingled with no laminar segregation, we found few double‐labeled neurons (≈5% of each singly labeled population). We also examined the development of FF and FB connections. FF connections were present at the earliest timepoint we examined (postnatal day 2, P2), while FB connections were not detectable until P11. Our findings indicate that, even in cortices without laminar segregation of FF and FB neurons, the two projection systems are largely distinct at the neuronal level and also differ with respect to the timing of their axonal outgrowth. J. Comp. Neurol. 519:3672–3683, 2011. © 2011 Wiley‐Liss, Inc.
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Studies of primate and rodent neuroanatomy indicate that forward and backward projections originate from separate cell populations, as PP requires.
“studies of primate and rodent neuroanatomy indicate that forward and backward projections originate from separate cell populations, 164 , 165 as PP requires.”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [165]
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Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex
Hubel, D. H., & Wiesel, T. N. (1962) · The Journal of Physiology · doi:10.1113/jphysiol.1962.sp006837 · Cited by 13,680 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Rao, R. P. N., & Ballard, D. H. (1999) · Nature Neuroscience · doi:10.1038/4580 · Cited by 5,483 · see citing works
Dynamic predictions: Oscillations and synchrony in top–down processing
Engel, A. K., Fries, P., & Singer, W. (2001) · Nature Reviews Neuroscience · doi:10.1038/35094565 · Cited by 3,454 · see citing works
Preface: Cerebral Cortex Has Come of Age
Goldman, P. S., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1-a · Cited by 3,412 · see citing works
Hierarchical models of object recognition in cortex
Riesenhuber, M., & Poggio, T. (1999) · Nature Neuroscience · doi:10.1038/14819 · Cited by 3,309 · see citing works
Das Reafferenzprinzip: Wechselwirkungen zwischen Zentralnervensystem und Peripherie
von Holst, E., & Mittelstaedt, H. (1950) · Naturwissenschaften · doi:10.1007/bf00622503 · Cited by 2,655 · see citing works
RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT
Hubel, D. H., & Wiesel, T. N. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.2.229 · Cited by 2,615 · see citing works
Neural basis of the spontaneous optokinetic response produced by visual inversion
Sperry, R. W. (1950) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0055479 · Cited by 1,789 · see citing works
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161 · see citing works
Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey
Rockland, K. S., & Pandya, D. Ν. (1979) · Brain Research · doi:10.1016/0006-8993(79)90485-2 · Cited by 1,076 · see citing works
On the computational architecture of the neocortex: II The role of cortico-cortical loops
Mumford, D. (1992) · Biological Cybernetics · doi:10.1007/bf00198477 · Cited by 1,074 · see citing works
On the computational architecture of the neocortex: I. The role of the thalamo-cortical loop
Mumford, D. (1991) · Biological Cybernetics · doi:10.1007/bf00202389 · Cited by 929 · see citing works
Specificity of monosynaptic connections from thalamus to visual cortex
Reid, R. C., & Alonso, J. (1995) · Nature · doi:10.1038/378281a0 · Cited by 732 · see citing works
Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model
Caviness, V. S., Takahashi, T., & Nowakowski, R. S. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93933-o · Cited by 566 · see citing works
Analysis of connectivity in the cat cerebral cortex
Scannell, J. W., Blakemore, C. B., & Mp, Y. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-02-01463.1995 · Cited by 554 · see citing works
Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex
Stettler, D. D., Das, A., Bennett, J., & Gilbert, C. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)01029-2 · Cited by 506 · see citing works
Area map of mouse visual cortex
Wang, Q., & Burkhalter, A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21286 · Cited by 498 · see citing works
Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia
Corfas, G., Roy, K., & Buxbaum, J. D. (2004) · Nature Neuroscience · doi:10.1038/nn1258 · Cited by 388 · see citing works
Density of neurons and synapses in the cerebral cortex of the mouse
Schüz, A., & Palm, G. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902860404 · Cited by 376 · see citing works
On counting and counting errors
Guillery, R. W. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10221 · Cited by 343 · see citing works
Takahashi, T., Goto, T., Miyama, S., Nowakowski, R. S., & Caviness, V. S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10357.1999 · Cited by 328 · see citing works
Roy, K., Murtie, J. C., El-Khodor, B. F., Edgar, N., Sardi, S. P., Hooks, B. M., Benoit-Marand, M., Chen, C., Moore, H., O'Donnell, P., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702157104 · Cited by 319 · see citing works
Barone, P., Batardiere, A., Knoblauch, K., & Kennedy, H. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03263.2000 · Cited by 300 · see citing works
Ontogenetic changes in the projections of neocortical neurons
Ivy, G., & Killackey, H. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-06-00735.1982 · Cited by 271 · see citing works
Corollary discharge dysfunction in schizophrenia: Can it explain auditory hallucinations?
Ford, J. M., & Mathalon, D. H. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.01.014 · Cited by 267 · see citing works
Hierarchical organization of areas in rat visual cortex
Coogan, T. A., & Burkhalter, A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03749.1993 · Cited by 260 · see citing works
Rockland, K. S., & Virga, A. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902850106 · Cited by 215 · see citing works
Rouiller, E. M., Simm, G., Villa, A. E. P., de Ribaupierre, Y., & de Ribaupierre, F. (1991) · Experimental Brain Research · doi:10.1007/bf00230523 · Cited by 201 · see citing works
Dima, D., Roiser, J. P., Dietrich, D. E., Bonnemann, C., Lanfermann, H., Emrich, H. M., & Dillo, W. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.03.033 · Cited by 192 · see citing works
Matin, L., Picoult, E., Stevens, J. K., et al. (1982) · Science · doi:10.1126/science.7063881 · Cited by 175 · see citing works
Development of Forward and Feedback Connections between Areas V1 and V2 of Human Visual Cortex
Burkhalter, A. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.5.476 · Cited by 166 · see citing works
Position Constancy during Pursuit Eye Movement: An Investigation of the Filehne Illusion
Mack, A., & Herman, E. (1973) · Quarterly Journal of Experimental Psychology · doi:10.1080/14640747308400324 · Cited by 138 · see citing works
Branching and laminar origin of projections between visual cortical areas in the cat
Bullier, J., Kennedy, H., & Salinger, W. L. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902280304 · Cited by 131 · see citing works
Impaired top-down processes in schizophrenia: a DCM study of ERPs
Dima, D., Dietrich, D. E., Dillo, W., & Emrich, H. M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.086 · Cited by 122 · see citing works
Conserved patterns of cortico-cortical connections define areal hierarchy in rat visual cortex
Coogan, T. A., & Burkhalter, A. (1990) · Experimental Brain Research · doi:10.1007/bf00228846 · Cited by 120 · see citing works
Gonchar, Y., & Burkhalter, A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10904.2003 · Cited by 114 · see citing works
Early Specification of the Hierarchical Organization of Visual Cortical Areas in the Macaque Monkey
Batardière, A. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.5.453 · Cited by 113 · see citing works
Shmuel, A., Korman, M., Sterkin, A., Harel, M., Ullman, S., Malach, R., & Grinvald, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4137-04.2005 · Cited by 110 · see citing works
Interchange of callosal and association projections in the developing visual cortex
Innocenti, G., Clarke, S., & Kraftsik, R. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-05-01384.1986 · Cited by 106 · see citing works
Schwartz, M. L., & Goldman, P. S. (1982) · Nature · doi:10.1038/299154a0 · Cited by 96 · see citing works
Mitchell, B. D., & Macklis, J. D. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20428 · Cited by 94 · see citing works
Sincich, L. C., & Horton, J. C. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05684.2003 · Cited by 85 · see citing works
Developmental Remodeling of Primate Visual Cortical Pathways
Barone, P., Dehay, C., Berland, M., Bullier, J., & Kennedy, H. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.1.22 · Cited by 82 · see citing works
Development of Inferior Temporal Cortex in the Monkey
Rodman, H. R. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.5.484 · Cited by 80 · see citing works
Laminar patterns of termination of cortico-cortical afferents in the somatosensory system
Friedman, D. P. (1983) · Brain Research · doi:10.1016/0006-8993(83)91103-4 · Cited by 70 · see citing works
Weisenhorn, D. M. V., Ilung, R. B., & Spatz, W. B. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903620207 · Cited by 59 · see citing works
Synaptic connection from cortical area V4 to V2 in macaque monkey
Anderson, J. C., & Martin, K. A. C. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.20914 · Cited by 56 · see citing works
Dong, H., Wang, Q., Valkova, K., Gonchar, Y., & Burkhalter, A. (2004) · Vision Research · doi:10.1016/j.visres.2004.09.007 · Cited by 49 · see citing works
Dong, H., Shao, Z., Nerbonne, J. M., & Burkhalter, A. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20164 · Cited by 41 · see citing works
Bai, W.-Z., Ishida, M., & Arimatsu, Y. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.08.056 · Cited by 32 · see citing works
Casanovas-Aguilar, C., Miró-Bernié, N., & Pérez‐Clausell, J. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00482-1 · Cited by 28 · see citing works
In vivo transcranial imaging of connections in mouse visual cortex
Wang, Q., Gao, E., & Burkhalter, A. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.07.024 · Cited by 25 · see citing works
Williams, L. E., Ramachandran, V. S., Hubbard, E. M., BRAFF, D. L., & Light, G. A. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.10.021 · Cited by 21 · see citing works
Pathway-Specific Utilization of Synaptic Zinc in the Macaque Ventral Visual Cortical Areas
Ichinohe, N., Matsushita, A., Ohta, K., & Rockland, K. S. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq028 · Cited by 18 · see citing works
Abnormal timing of visual feedback processing in young adults with schizophrenia
Kemner, C., Foxe, J. J., Tankink, J. E., Kahn, R. S., & Lamme, V. A. F. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.07.009 · Cited by 17 · see citing works
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
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Harris, K. D., & Shepherd, G. M. G. (2015) · Nature Neuroscience · doi:10.1038/nn.3917 · Cited by 1,215 · see citing works
Functional specialization of mouse higher visual cortical areas
Andermann, M. L., Kerlin, A. M., Roumis, D. K., Glickfeld, L. L., & Reid, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.11.013 · Cited by 406 · see citing works
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Dehay, C., Kennedy, H., & Kosik, K. S. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.060 · Cited by 314 · see citing works
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- Authors
- Berezovskii, V. K., Nassi, J. J., & Born, R. T.
- Affiliations
- Harvard University (US)
- Corresponding author
- Born, Richard T.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2011-10-17
- Volume
- 519
- Issue
- 18
- Pages
- 3672-3683
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC3219532
- OpenAlex
- W2150908684
- Cited by
- 84
- References
- 59
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 7 · 2023: 7 · 2022: 7 · 2021: 7 · 2020: 5 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 8 · 2015: 3 · 2014: 3 · 2013: 4 · 2012: 3
- FWCI
- 2.11
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Eye Institute (R01EY011379, EY12196, P30EY012196)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- feedback projections, mouse visual cortex, cortical hierarchy, retrograde tracing, area 17, axon growth, postnatal development, corticocortical connections
- MeSH terms
- Animals, Axons, Brain Mapping, Mice, Inbred C57BL, Neural Inhibition, Visual Cortex, Visual Pathways, Mice, Neuroanatomical Tract-Tracing Techniques
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