Border-ownership tuning determines the connectivity between V4 and V1 in the macaque visual system.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
23 Oct 2024
23 Oct 2024
Historique:
received:
12
10
2023
accepted:
07
10
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
Cortical feedback connections are extremely numerous but the logic of connectivity between higher and lower areas remains poorly understood. Feedback from higher visual areas to primary visual cortex (V1) has been shown to enhance responses on perceptual figures compared to backgrounds, an effect known as figure-background modulation (FBM). A likely source of this feedback are border-ownership (BO) selective cells in mid-tier visual areas (e.g. V4) which represent the location of figures. We examined the connectivity between V4 cells and V1 cells using noise-correlations and micro-stimulation to estimate connectivity strength. We show that connectivity is consistent with a model in which BO-tuned V4 cells send positive feedback in the direction of their preferred figure and negative feedback in the opposite direction. This connectivity scheme can recreate patterns of FBM observed in previous studies. These results provide insights into the cortical connectivity underlying figure-background perception and establish a link between FBM and BO-tuning.
Identifiants
pubmed: 39438464
doi: 10.1038/s41467-024-53256-8
pii: 10.1038/s41467-024-53256-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9115Informations de copyright
© 2024. The Author(s).
Références
Roelfsema, P. R. Cortical algorithms for perceptual grouping. Annu. Rev. Neurosci. 29, 203–227 (2006).
pubmed: 16776584
doi: 10.1146/annurev.neuro.29.051605.112939
Bullier, J. Integrated model of visual processing. Brain Res. Rev. 36, 96–107 (2001).
pubmed: 11690606
doi: 10.1016/S0165-0173(01)00085-6
Keller, G. B. & Mrsic-Flogel, T. D. Predictive processing: a canonical cortical computation. Neuron 100, 424–435 (2018).
pubmed: 30359606
pmcid: 6400266
doi: 10.1016/j.neuron.2018.10.003
Lamme, V. A. The neurophysiology of figure-ground segregation in primary visual cortex. J. Neurosci. 15, 1605–1615 (1995).
pubmed: 7869121
pmcid: 6577835
doi: 10.1523/JNEUROSCI.15-02-01605.1995
Zipser, K., Lamme, V. A. & Schiller, P. H. Contextual modulation in primary visual cortex. J. Neurosci. 16, 7376–7389 (1996).
pubmed: 8929444
pmcid: 6578953
doi: 10.1523/JNEUROSCI.16-22-07376.1996
Poort, J., Self, M. W., Van Vugt, B., Malkki, H. & Roelfsema, P. R. Texture segregation causes early figure enhancement and later ground suppression in areas V1 and V4 of visual cortex. Cereb. Cortex 26, 3964–3976 (2016).
pubmed: 27522074
pmcid: 5028009
doi: 10.1093/cercor/bhw235
Self, M. W. et al. The segmentation of proto-objects in the monkey primary visual cortex. Curr. Biol. 29, 1019–1029.e4 (2019).
pubmed: 30853432
doi: 10.1016/j.cub.2019.02.016
Self, M. W., van Kerkoerle, T., Supèr, H. & Roelfsema, P. R. Distinct roles of the cortical layers of area V1 in figure-ground segregation. Curr. Biol. 23, 2121–2129 (2013).
pubmed: 24139742
doi: 10.1016/j.cub.2013.09.013
Klink, P. C., Dagnino, B., Gariel-Mathis, M.-A. & Roelfsema, P. R. Distinct feedforward and feedback effects of microstimulation in visual cortex reveal neural mechanisms of texture segregation. Neuron 95, 209–220.e3 (2017).
pubmed: 28625487
doi: 10.1016/j.neuron.2017.05.033
Lamme, V. A., Zipser, K. & Spekreijse, H. Figure-ground activity in primary visual cortex is suppressed by anesthesia. Proc. Natl. Acad. Sci. USA 95, 3263–3268 (1998).
pubmed: 9501251
pmcid: 19730
doi: 10.1073/pnas.95.6.3263
Chen, M. et al. Incremental integration of global contours through interplay between visual cortical areas. Neuron 82, 682–694 (2014).
pubmed: 24811385
doi: 10.1016/j.neuron.2014.03.023
Kirchberger, L. et al. The essential role of recurrent processing for figure-ground perception in mice. Sci. Adv. 7, eabe1833 (2021).
pubmed: 34193411
pmcid: 8245045
doi: 10.1126/sciadv.abe1833
Zhou, H., Friedman, H. S. & von der Heydt, R. Coding of border ownership in monkey visual cortex. J. Neurosci. 20, 6594–6611 (2000).
pubmed: 10964965
pmcid: 4784717
doi: 10.1523/JNEUROSCI.20-17-06594.2000
Qiu, F. T. & von der Heydt, R. Figure and ground in the visual cortex: V2 combines stereoscopic cues with Gestalt rules. Neuron 47, 155–156 (2005).
pubmed: 15996555
pmcid: 1564069
doi: 10.1016/j.neuron.2005.05.028
Marques, T., Nguyen, J., Fioreze, G. & Petreanu, L. The functional organization of cortical feedback inputs to primary visual cortex. Nat. Neurosci. 21, 757–764 (2018).
pubmed: 29662217
doi: 10.1038/s41593-018-0135-z
Franken, T. P. & Reynolds, J. H. Columnar processing of border ownership in primate visual cortex. Elife 10, e72573 (2021).
pubmed: 34845986
pmcid: 8631947
doi: 10.7554/eLife.72573
Hesse, J. K. & Tsao, D. Y. Functional modules for visual scene segmentation in macaque visual cortex. Proc. Natl. Acad. Sci. USA 120, e2221122120 (2023).
pubmed: 37523552
pmcid: 10410728
doi: 10.1073/pnas.2221122120
Supèr, H. & Roelfsema, P. R. Chronic multiunit recordings in behaving animals: advantages and limitations. Prog. Brain Res. 147, 263–282 (2005).
pubmed: 15581712
doi: 10.1016/S0079-6123(04)47020-4
Cohen, M. R. & Maunsell, J. H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12, 1594–1600 (2009).
pubmed: 19915566
pmcid: 2820564
doi: 10.1038/nn.2439
Palmer, C., Cheng, S.-Y. & Seidemann, E. Linking neuronal and behavioral performance in a reaction-time visual detection task. J. Neurosci. 27, 8122–8137 (2007).
pubmed: 17652603
pmcid: 2198904
doi: 10.1523/JNEUROSCI.1940-07.2007
Trautmann, E. M. et al. Accurate estimation of neural population dynamics without spike sorting. Neuron 103, 292–308.e4 (2019).
pubmed: 31171448
pmcid: 7002296
doi: 10.1016/j.neuron.2019.05.003
Self, M. W., Kooijmans, R. N., Supèr, H., Lamme, V. A. & Roelfsema, P. R. Different glutamate receptors convey feedforward and recurrent processing in macaque V1. Proc. Natl. Acad. Sci. USA 109, 11031–11036 (2012).
pubmed: 22615394
pmcid: 3390882
doi: 10.1073/pnas.1119527109
Roelfsema, P. R., Engel, A. K., König, P. & Singer, W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157–161 (1997).
pubmed: 8990118
doi: 10.1038/385157a0
Smith, M. A. & Kohn, A. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28, 12591–12603 (2008).
pubmed: 19036953
pmcid: 2656500
doi: 10.1523/JNEUROSCI.2929-08.2008
Cohen, M. R. & Kohn, A. Measuring and interpreting neuronal correlations. Nat. Neurosci. 14, 811–819 (2011).
pubmed: 21709677
pmcid: 3586814
doi: 10.1038/nn.2842
Shadlen, M. N. & Newsome, W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998).
pubmed: 9570816
pmcid: 6793166
doi: 10.1523/JNEUROSCI.18-10-03870.1998
Kenet, T., Bibitchkov, D., Tsodyks, M., Grinvald, A. & Arieli, A. Spontaneously emerging cortical representations of visual attributes. Nature 425, 954–956 (2003).
pubmed: 14586468
doi: 10.1038/nature02078
Lin, I.-C., Okun, M., Carandini, M. & Harris, K. D. The nature of shared cortical variability. Neuron 87, 644–656 (2015).
pubmed: 26212710
pmcid: 4534383
doi: 10.1016/j.neuron.2015.06.035
Ringach, D. L. Spontaneous and driven cortical activity: implications for computation. Curr. Opin. Neurobiol. 19, 439–444 (2009).
pubmed: 19647992
pmcid: 3319344
doi: 10.1016/j.conb.2009.07.005
Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011).
pubmed: 21478872
pmcid: 3089591
doi: 10.1038/nature09880
Moeller, S., Freiwald, W. A. & Tsao, D. Y. Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 320, 1355–1359 (2008).
pubmed: 18535247
pmcid: 8344042
doi: 10.1126/science.1157436
Roelfsema, P. R., Lamme, V. A. & Spekreijse, H. Synchrony and covariation of firing rates in the primary visual cortex during contour grouping. Nat. Neurosci. 7, 982–991 (2004).
pubmed: 15322549
doi: 10.1038/nn1304
Reimer, J. et al. Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84, 355–362 (2014).
pubmed: 25374359
pmcid: 4323337
doi: 10.1016/j.neuron.2014.09.033
Hasselmo, M. E. & Sarter, M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36, 52–73 (2011).
pubmed: 20668433
doi: 10.1038/npp.2010.104
Rossi, A. F., Rittenhouse, C. D. & Paradiso, M. A. The representation of brightness in primary visual cortex. Science 273, 1104–1107 (1996).
pubmed: 8688096
doi: 10.1126/science.273.5278.1104
Lamme, V. A. & Roelfsema, P. R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571–579 (2000).
pubmed: 11074267
doi: 10.1016/S0166-2236(00)01657-X
Self, M. W., Mookhoek, A., Tjalma, N. & Roelfsema, P. R. Contextual effects on perceived contrast: figure-ground assignment and orientation contrast. J. Vis. 15, 2 (2015).
pubmed: 25645435
doi: 10.1167/15.2.2
Poort, J. et al. The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex. Neuron 75, 143–156 (2012).
pubmed: 22794268
doi: 10.1016/j.neuron.2012.04.032
Qiu, F. T. & von der Heydt, R. Neural representation of transparent overlay. Nat. Neurosci. 10, 283–284 (2007).
pubmed: 17310247
pmcid: 1820980
doi: 10.1038/nn1853
Hesse, J. K. & Tsao, D. Y. Consistency of border-ownership cells across artificial stimuli, natural stimuli, and stimuli with ambiguous contours. J. Neurosci. 36, 11338–11349 (2016).
pubmed: 27807174
pmcid: 6601962
doi: 10.1523/JNEUROSCI.1857-16.2016
Williford, J. R. & von der Heydt, R. Figure-ground organization in visual cortex for natural scenes. eNeuro 3, ENEURO.0127–16.2016 (2016).
pubmed: 28058269
doi: 10.1523/ENEURO.0127-16.2016
Likova, L. T. & Tyler, C. W. Occipital network for figure/ground organization. Exp. Brain Res. 189, 257–267 (2008).
pubmed: 18604528
doi: 10.1007/s00221-008-1417-6
Rockland, K. S. & Pandya, D. N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research 179, 3–20 (1979).
pubmed: 116716
doi: 10.1016/0006-8993(79)90485-2
Rockland, K. S., Saleem, K. S. & Tanaka, K. Divergent feedback connections from areas V4 and TEO in the macaque. Visual Neuroscience 11, 579–600 (1994).
pubmed: 8038130
doi: 10.1017/S0952523800002480
Anderson, J. C. & Martin, K. A. The synaptic connections between cortical areas V1 and V2 in macaque monkey. J. Neurosci. 29, 11283–11293 (2009).
pubmed: 19741135
pmcid: 6665918
doi: 10.1523/JNEUROSCI.5757-08.2009
Markov, N. T. et al. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 24, 17–36 (2014).
pubmed: 23010748
doi: 10.1093/cercor/bhs270
Craft, E., Schütze, H., Niebur, E., von der Heydt, R. & Schutze, H. A Neural Model of Figure-Ground Organization. J. Neurophysiol. 97, 4310–4326 (2007).
pubmed: 17442769
doi: 10.1152/jn.00203.2007
Jehee, J. F., Lamme, V. A. & Roelfsema, P. R. Boundary assignment in a recurrent network architecture. Vision Res 47, 1153–1165 (2007).
pubmed: 17368500
doi: 10.1016/j.visres.2006.12.018
Angelucci, A., Levitt, J. B. & Lund, J. S. Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. Progress in Brain Research 136, 373–388 (2002).
pubmed: 12143395
doi: 10.1016/S0079-6123(02)36031-X
Munk, M. H., Nowak, L. G., Nelson, J. I. & Bullier, J. Structural basis of cortical synchronization. II. Effects of cortical lesions. Journal of Neurophysiology 74, 2401–2414 (1995).
pubmed: 8747201
doi: 10.1152/jn.1995.74.6.2401
Fişek, M. et al. Cortico-cortical feedback engages active dendrites in visual cortex. Nature 617, 769–776 (2023).
pubmed: 37138089
pmcid: 10244179
doi: 10.1038/s41586-023-06007-6
de Vries, S. E. J. et al. A large-scale standardized physiological survey reveals functional organization of the mouse visual cortex. Nat. Neurosci. 23, 138–151 (2020).
pubmed: 31844315
doi: 10.1038/s41593-019-0550-9
Zhang, S. et al. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660–665 (2014).
pubmed: 25104383
pmcid: 5776147
doi: 10.1126/science.1254126
McFarland, J. M., Bondy, A. G., Cumming, B. G. & Butts, D. A. High-resolution eye tracking using V1 neuron activity. Nat. Commun. 5, 4605 (2014).
pubmed: 25197783
doi: 10.1038/ncomms5605
Bondy, A. G., Haefner, R. M. & Cumming, B. G. Feedback determines the structure of correlated variability in primary visual cortex. Nat. Neurosci. 21, 598–606 (2018).
pubmed: 29483663
pmcid: 5876152
doi: 10.1038/s41593-018-0089-1
Nienborg, H. & Cumming, B. Correlations between the activity of sensory neurons and behavior: how much do they tell us about a neuron’s causality? Curr. Opin. Neurobiol. 20, 376–381 (2010).
pubmed: 20545019
pmcid: 2952283
doi: 10.1016/j.conb.2010.05.002
Bair, W., Zohary, E. & Newsome, W. T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676–1697 (2001).
pubmed: 11222658
pmcid: 6762960
doi: 10.1523/JNEUROSCI.21-05-01676.2001
Shipp, S. The functional logic of cortico-pulvinar connections. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 1605–1624 (2003).
pubmed: 14561322
pmcid: 1693262
doi: 10.1098/rstb.2002.1213
Sherman, S. M. & Guillery, R. W. On the actions that one nerve cell can have on another: distinguishing ‘drivers’ from ‘modulators’. Proc. Natl. Acad. Sci. USA 95, 7121–7126 (1998).
pubmed: 9618549
pmcid: 22761
doi: 10.1073/pnas.95.12.7121
D’Souza, R. D., Meier, A. M., Bista, P., Wang, Q. & Burkhalter, A. Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas. Elife 5, e19332 (2016).
pubmed: 27669144
pmcid: 5074802
doi: 10.7554/eLife.19332
Vangeneugden, J. et al. Activity in lateral visual areas contributes to surround suppression in awake mouse V1. Curr. Biol. 29, 4268–4275.e7 (2019).
pubmed: 31786063
doi: 10.1016/j.cub.2019.10.037
Nurminen, L., Merlin, S., Bijanzadeh, M., Federer, F. & Angelucci, A. Top-down feedback controls spatial summation and response amplitude in primate visual cortex. Nat. Commun. 9, 2281 (2018).
pubmed: 29892057
pmcid: 5995810
doi: 10.1038/s41467-018-04500-5
Shao, Z. & Burkhalter, A. Different balance of excitation and inhibition in forward and feedback circuits of rat visual cortex. J. Neurosci. 16, 7353–7365 (1996).
pubmed: 8929442
pmcid: 6578929
doi: 10.1523/JNEUROSCI.16-22-07353.1996
Gonchar, Y. & Burkhalter, A. Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J. Neurosci. 23, 10904–10912 (2003).
pubmed: 14645486
pmcid: 6740993
doi: 10.1523/JNEUROSCI.23-34-10904.2003
Nassi, J. J., Lomber, S. G. & Born, R. T. Corticocortical feedback contributes to surround suppression in V1 of the alert primate. J. Neurosci. 33, 8504–8517 (2013).
pubmed: 23658187
pmcid: 3690087
doi: 10.1523/JNEUROSCI.5124-12.2013
Salin, P. A. & Bullier, J. Corticocortical connections in the visual system: structure and function. Physiol. Rev. 75, 107–154 (1995).
pubmed: 7831395
doi: 10.1152/physrev.1995.75.1.107
Williams, P. E., Mechler, F., Gordon, J., Shapley, R. & Hawken, M. J. Entrainment to video displays in primary visual cortex of macaque and humans. J. Neurosci. 24, 8278–8288 (2004).
pubmed: 15385611
pmcid: 6729686
doi: 10.1523/JNEUROSCI.2716-04.2004
BorderOwnership v1.0.0 https://doi.org/10.5281/zenodo.13378939