Feedforward, feedback and inhibitory connections in primate visual cortex
Abstract
Visual cortical circuits are organized at multiple levels of complexity including cortical areas, layers and columns, and specific cell types within these modules. Making sense of the functions of these circuits from anatomical observations requires linking these circuits to function at each of these levels of complexity. Observations of these relationships have become increasingly sophisticated over the last several decades, beginning with correlations between the connectivities and functions of various visual cortical areas and progressing toward cell type-specificity. These studies have informed current views about the functional interactions between cortical areas and modules and the mechanisms by which fine scale microcircuits influence interactions at more coarse levels of organization.
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Feedback connections tend to terminate in distinct layers of cortex relative to the feedforward ones making the idea of separate but interacting networks for recognition and generation potentially attractive.
“Feedback connections tend to terminate in distinct layers of cortex relative to the feedforward ones (Felleman and Van Essen, 1991; Callaway, 2004) making the idea of separate but interacting networks for recognition and generation potentially attractive34.”
From Toward an integration of deep learning and neuroscience (2016) · cites this paper as Callaway, 2004
Cites
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
Receptive fields and functional architecture of monkey striate cortex
Hubel, D. H., & Wiesel, T. N. (1968) · The Journal of Physiology · doi:10.1113/jphysiol.1968.sp008455 · Cited by 6,520 · 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
Segregation of Form, Color, Movement, and Depth: Anatomy, Physiology, and Perception
Livingstone, M. S., & Hubel, D. H. (1988) · Science · doi:10.1126/science.3283936 · Cited by 3,358 · see citing works
Maunsell, J., & van Essen, D. (1983) · The Journal of Neuroscience · doi:10.1523/jneurosci.03-12-02563.1983 · Cited by 1,602 · see citing works
Two networks of electrically coupled inhibitory neurons in neocortex
Gibson, J. R., Beierlein, M., & Connors, B. W. (1999) · Nature · doi:10.1038/47035 · Cited by 1,404 · see citing works
Direction and orientation selectivity of neurons in visual area MT of the macaque
Albright, T. D. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.52.6.1106 · Cited by 1,089 · see citing works
Hierarchical organization and functional streams in the visual cortex
Van Essen, D. C., & Maunsell, J. H. R. (1983) · Trends in Neurosciences · doi:10.1016/0166-2236(83)90167-4 · Cited by 962 · see citing works
Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey
Hubel, D. H., & Wiesel, T. N. (1972) · The Journal of Comparative Neurology · doi:10.1002/cne.901460402 · Cited by 945 · see citing works
Somogyi, P., Tamás, G., Luján, R., & Buhl, E. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00061-1 · Cited by 860 · see citing works
On the actions that one nerve cell can have on another: distinguishing “drivers” from “modulators”
Sherman, S. M., & Guillery, R. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.7121 · Cited by 746 · cited 1× · see citing works
“Some connections appear to have a dominant, driving influence while others are modulatory (Callaway, 1998; Crick & Koch, 1998; Sherman & Guillery, 1998).”
BackgroundLund, J. S., Lund, R. D., Hendrickson, A. E., Milam, A. H., & Fuchs, A. F. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901640303 · Cited by 681 · see citing works
Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons
Tamás, G., Buhl, E. H., Lörincz, A., & Somogyi, P. (2000) · Nature Neuroscience · doi:10.1038/73936 · Cited by 648 · see citing works
Corticocortical connections in the visual system: structure and function
Salin, P. A., & Bullier, J. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.1.107 · Cited by 639 · see citing works
Thalamic Relay Functions and Their Role in Corticocortical Communication
Guillery, R. W., & Sherman, S. M. (2002) · Neuron · doi:10.1016/s0896-6273(01)00582-7 · Cited by 637 · see citing works
LOCAL CIRCUITS IN PRIMARY VISUAL CORTEX OF THE MACAQUE MONKEY
Callaway, E. M. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.47 · Cited by 603 · see citing works
Self-citationTermination of afferent axons in macaque striate cortex
Blasdel, G. G., & Lund, J. S. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-07-01389.1983 · Cited by 452 · see citing works
Wiesel, T. N., Hubel, D. H., & Lam, D. M.-K. (1974) · Brain Research · doi:10.1016/0006-8993(74)90416-8 · Cited by 436 · see citing works
Troyer, T. W., Krukowski, A. E., Priebe, N. J., & Miller, K. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-15-05908.1998 · Cited by 429 · see citing works
Henderickson, A. E., Wilson, J. R., & Ogren, M. P. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901820108 · Cited by 423 · see citing works
The functional logic of cortico-pulvinar connections
Shipp, S. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1213 · Cited by 411 · cited 1× · see citing works
“And the relatively precise and systematic organization of connections to and from the cortex and pulvinar (see (Shipp, 2003) for review) suggest that these connections are likely to mediate relatively direct interactions between cortical areas.”
BackgroundKawaguchi, Y., & Kondo, S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024126110356 · Cited by 395 · see citing works
Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Swadlow, H. A. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.1.25 · Cited by 354 · see citing works
Constraints on cortical and thalamic projections: the no-strong-loops hypothesis
Crick, F., & Koch, C. (1998) · Nature · doi:10.1038/34584 · Cited by 353 · cited 2× · see citing works
“Some connections appear to have a dominant, driving influence while others are modulatory (Callaway, 1998; Crick & Koch, 1998; Sherman & Guillery, 1998).”
BackgroundAgmon, A., & Connors, B. W. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00319.1992 · Cited by 345 · see citing works
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344 · see citing works
Physiological organization of layer 4 in macaque striate cortex
Blasdel, G. G., & Fitzpatrick, D. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-03-00880.1984 · Cited by 310 · see citing works
Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons
Dantzker, J. L. M., & Callaway, E. M. (2000) · Nature Neuroscience · doi:10.1038/76656 · Cited by 303 · see citing works
Self-citationShapley, R. M., Hawken, M. J., & Ringach, D. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00332-5 · Cited by 263 · see citing works
Parallel colour-opponent pathways to primary visual cortex
Chatterjee, S., & Callaway, E. M. (2003) · Nature · doi:10.1038/nature02167 · Cited by 255 · see citing works
Self-citationFreund, T. F., Martin, K. A. C., Soltész, I., Somogyi, P., & Whitteridge, D. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890211 · Cited by 197 · see citing works
Parallel pathways in macaque monkey striate cortex: anatomically defined columns in layer III.
Lachica, E. A., Beck, P. D., & Casagrande, V. A. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.8.3566 · Cited by 189 · see citing works
Meskenaïte, V. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970303)379:1 · Cited by 180 · see citing works
Concurrent processing in the primate visual cortex.
Essen, D. C. V., & DeYoe, E. A. (1995) · Cited by 179 · see citing works
Functionally distinct inhibitory neurons at the first stage of visual cortical processing
Hirsch, J. A., Martinez, L. M., Pillai, C., Alonso, J.-M., Wang, Q., & Sommer, F. T. (2003) · Nature Neuroscience · doi:10.1038/nn1152 · Cited by 176 · see citing works
Yabuta, N. H., & Callaway, E. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-22-09489.1998 · Cited by 131 · see citing works
Self-citationEdwards, D. P., Purpura, K. P., & Kaplan, E. (1995) · Vision Research · doi:10.1016/0042-6989(94)00253-i · Cited by 117 · see citing works
Connectivity of GABAergic Calretinin-immunoreactive Neurons in Rat Primary Visual Cortex
Gonchar, Y. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.7.683 · Cited by 117 · 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
Callaway, E. M., & Wiser, A. K. (1996) · Visual Neuroscience · doi:10.1017/s0952523800009159 · Cited by 112 · see citing works
Self-citationThalamocortical control of feed–forward inhibition in awake somatosensory ‘barrel’ cortex
Swadlow, H. A. (2002) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1156 · Cited by 107 · see citing works
Wiser, A., & Callaway, E. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02724.1996 · Cited by 99 · see citing works
Self-citationFries, W., Keizer, K., & Kuypers, H. G. J. M. (1985) · Experimental Brain Research · doi:10.1007/bf00235878 · Cited by 89 · see citing works
Layer-Specific Input to Distinct Cell Types in Layer 6 of Monkey Primary Visual Cortex
Briggs, F., & Callaway, E. M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03600.2001 · Cited by 87 · see citing works
Self-citationSawatari, A., & Callaway, E. M. (2000) · Neuron · doi:10.1016/s0896-6273(00)80908-3 · Cited by 76 · see citing works
Self-citationVruwink, M., Schmidt, H. H. H. W., Weinberg, R. J., & Burette, A. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1413 · Cited by 72 · see citing works
Benevento, L. A., & Standage, G. P. (1982) · Brain Research · doi:10.1016/0006-8993(82)90991-x · Cited by 55 · see citing works
LGN Input to Simple Cells and Contrast-Invariant Orientation Tuning: An Analysis
Troyer, T. W., Krukowski, A. E., & Miller, K. D. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.87.6.2741 · Cited by 53 · see citing works
Wiser, A. K., & Callaway, E. M. (1997) · Visual Neuroscience · doi:10.1017/s095252380001138x · Cited by 19 · see citing works
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Larkum, M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.006 · Cited by 755 · see citing works
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Spaak, E., Bonnefond, M., Maier, A., Leopold, D. A., & Jensen, O. (2012) · Current Biology · doi:10.1016/j.cub.2012.10.020 · Cited by 385 · see citing works
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Weiler, N., Wood, L., Yu, J., Solla, S. A., & Shepherd, G. M. G. (2008) · Nature Neuroscience · doi:10.1038/nn2049 · Cited by 330 · see citing works
Haeusler, S., & Maass, W. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj132 · Cited by 221 · see citing works
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Olman, C. A., Harel, N., Feinberg, D. A., He, S., Zhang, P., Ugurbil, K., & Yacoub, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032536 · Cited by 194 · see citing works
Mangia, S., Giove, F., Tkáč, I., Logothetis, N. K., Henry, P.-G., Olman, C. A., Maraviglia, B., Di Salle, F., & Uğurbil, K. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.134 · Cited by 161 · see citing works
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- Authors
- Callaway, E. M.
- Affiliations
- Salk Institute for Biological Studies (US)
- Corresponding author
- Callaway, Edward M
- ORCID
- Callaway, Edward M
- Venue
- Neural Networks
- Publisher
- Elsevier BV
- Published
- 2004-06
- Volume
- 17
- Issue
- 5-6
- Pages
- 625-632
- ISSN
- 0893-6080 (ISSN-L)
- OpenAlex
- W2000308859
- Cited by
- 165
- References
- 49
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 9 · 2023: 6 · 2022: 6 · 2021: 9 · 2020: 6 · 2019: 8 · 2018: 7 · 2017: 7 · 2016: 9 · 2015: 9 · 2014: 7 · 2013: 14 · 2012: 8
- FWCI
- 0.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neural Networks (publishedVersion)
- PubMed (publishedVersion)
- 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 › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- primate visual cortex, feedforward connections, feedback connections, inhibitory connections, cortical circuits, cortical layers, cortical columns, cell type specificity, microcircuits, functional interactions
- MeSH terms
- Animals, Feedback, Neural Inhibition, Neurons, Primates, Visual Cortex, Visual Pathways, Neural Networks, Computer
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