Abstract
According to recent models of visuo-spatial processing, the medial parieto-occipital cortex is a crucial node of the dorsal visual stream. Evidence from neurophysiological studies in monkeys has indicated that the parieto-occipital sulcus (POS) contains three functionally and cytoarchitectonically distinct areas: the visual area V6 in the fundus of the POS, and the visuo-motor areas V6Av and V6Ad in a progressively dorsal and anterior location with respect to V6. Besides different topographical organization, cytoarchitectonics, and functional properties, these three monkey areas can also be distinguished based on their patterns of cortico-cortical connections. Thanks to wide-field retinotopic mapping, areas V6 and V6Av have been also mapped in the human brain. Here, using a combined approach of resting-state functional connectivity and task-evoked activity by fMRI, we identified a new region in the anterior POS showing a pattern of functional properties and cortical connections that suggests a homology with the monkey area V6Ad. In addition, we observed distinct patterns of cortical connections associated with the human V6 and V6Av which are remarkably consistent with those showed by the anatomical tracing studies in the corresponding monkey areas. Consistent with recent models on visuo-spatial processing, our findings demonstrate a gradient of functional specialization and cortical connections within the human POS, with more posterior regions primarily dedicated to the analysis of visual attributes useful for spatial navigation and more anterior regions primarily dedicated to analyses of spatial information relevant for goal-directed action.
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References
Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J Neurosci 23(11):4689–4699 pii 23/11/4689
Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37(1):90–101. doi:10.1016/j.neuroimage.2007.04.042
Beurze SM, de Lange FP, Toni I, Medendorp WP (2009) Spatial and effector processing in the human parietofrontal network for reaches and saccades. J Neurophysiol 101(6):3053–3062. doi:10.1152/jn.91194.2008
Bremmer F, Schlack A, Shah NJ, Zafiris O, Kubischik M, Hoffmann K, Zilles K, Fink GR (2001) Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29(1):287–296
Cardin V, Smith AT (2010) Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb Cortex 20(8):1964–1973. doi:10.1093/cercor/bhp268
Cardin V, Smith AT (2011) Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion. J Neurophysiol 106(3):1240–1249. doi:10.1152/jn.01120.2010
Chumbley J, Worsley K, Flandin G, Friston K (2010) Topological FDR for neuroimaging. Neuroimage 49(4):3057–3064. doi:10.1016/j.neuroimage.2009.10.090
Connolly JD, Andersen RA, Goodale MA (2003) FMRI evidence for a ‘parietal reach region’ in the human brain. Exp Brain Res 153(2):140–145. doi:10.1007/s00221-003-1587-1
Culham JC, Danckert SL, DeSouza JF, Gati JS, Menon RS, Goodale MA (2003) Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153(2):180–189. doi:10.1007/s00221-003-1591-5
Culham JC, Cavina-Pratesi C, Singhal A (2006) The role of parietal cortex in visuomotor control: what have we learned from neuroimaging? Neuropsychologia 44(13):2668–2684. doi:10.1016/j.neuropsychologia.2005.11.003
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601. doi:10.1038/33402
Fattori P, Gamberini M, Kutz DF, Galletti C (2001) ‘Arm-reaching’ neurons in the parietal area V6A of the macaque monkey. Eur J Neurosci 13(12):2309–2313
Fattori P, Kutz DF, Breveglieri R, Marzocchi N, Galletti C (2005) Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey. Eur J Neurosci 22(4):956–972. doi:10.1111/j.1460-9568.2005.04288.x
Fattori P, Pitzalis S, Galletti C (2009a) The cortical visual area V6 in macaque and human brains. J Physiol Paris 103:88–97
Fattori P, Breveglieri R, Marzocchi N, Filippini D, Bosco A, Galletti C (2009b) Hand orientation during reach-to-grasp movements modulates neuronal activity in the medial posterior parietal area V6A. J Neurosci 29(6):1928–1936. doi:10.1523/JNEUROSCI.4998-08.2009
Filimon F, Nelson JD, Huang RS, Sereno MI (2009) Multiple parietal reach regions in humans: cortical representations for visual and proprioceptive feedback during on-line reaching. J Neurosci 29(9):2961–2971. doi:10.1523/JNEUROSCI.3211-08.2009
Fischl B, Sereno MI, Tootell RB, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8(4):272–284. doi:10.1002/(SICI)1097-0193(1999)8:4<272::AID-HBM10>3.0.CO;2-4
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711. doi:10.1038/nrn2201
Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1995) Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4:23–235
Furlan M, Wann JP, Smith AT (2013) A representation of changing heading direction in human cortical areas pVIP and CSv. Cereb Cortex. doi:10.1093/cercor/bht132
Galati G, Committeri G, Pitzalis S, Pelle G, Patria F, Fattori P, Galletti C (2011) Intentional signals during saccadic and reaching delays in the human posterior parietal cortex. Eur J Neurosci 34(11):1871–1885. doi:10.1111/j.1460-9568.2011.07885.x
Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8(1):30–52
Galletti C, Fattori P, Kutz DF, Battaglini PP (1997) Arm movement-related neurons in the visual area V6A of the macaque superior parietal lobule. Eur J Neurosci 9(2):410–413
Galletti C, Fattori P, Gamberini M, Kutz DF (1999a) The cortical visual area V6: brain location and visual topography. Eur J Neurosci 11(11):3922–3936
Galletti C, Fattori P, Kutz DF, Gamberini M (1999b) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11(2):575–582
Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M (2001) The cortical connections of area V6: an occipito-parietal network processing visual information. Eur J Neurosci 13(8):1572–1588
Galletti C, Kutz DF, Gamberini M, Breveglieri R, Fattori P (2003) Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153(2):158–170. doi:10.1007/s00221-003-1589-z
Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C (2009) Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513(6):622–642. doi:10.1002/cne.21980
Gamberini M, Galletti C, Bosco A, Breveglieri R, Fattori P (2011) Is the medial posterior parietal area V6A a single functional area? J Neurosci 31(13):5145–5157. doi:10.1523/JNEUROSCI.5489-10.2011
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25. doi:10.1016/0166-2236(92)90344-8
Hasson U, Harel M, Levy I, Malach R (2003) Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37(6):1027–1041
Kolster H, Peeters R, Orban GA (2010) The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. J Neurosci 30(29):9801–9820. doi:10.1523/JNEUROSCI.2069-10.2010
Konen CS, Mruczek RE, Montoya JL, Kastner S (2013) Functional organization of human posterior parietal cortex: grasping- and reaching-related activations relative to topographically organized cortex. J Neurophysiol 109(12):2897–2908. doi:10.1152/jn.00657.2012
Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12(4):217–230. doi:10.1038/nrn3008
Kutz DF, Fattori P, Gamberini M, Breveglieri R, Galletti C (2003) Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey. Exp Brain Res 149(1):83–95. doi:10.1007/s00221-002-1337-9
Levy I, Hasson U, Avidan G, Hendler T, Malach R (2001) Center-periphery organization of human object areas. Nat Neurosci 4(5):533–539. doi:10.1038/87490
Luppino G, Ben Hamed S, Gamberini M, Matelli M, Galletti C (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21(11):3056–3076. doi:10.1111/j.1460-9568.2005.04149
Malach R, Levy I, Hasson U (2002) The topography of high-order human object areas. Trends Cogn Sci 6(4):176–184 pii S1364661302018703
Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106(47):20069–20074. doi:10.1073/pnas.0905314106
Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J (1995) A probabilistic atlas of the human brain: theory and rationale for its development. International Consortium for Brain Mapping (ICBM). Neuroimage 2(2):89–101 pii S1053811985710129
Morrone MC, Tosetti M, Montanaro D, Fiorentini A, Cioni G, Burr DC (2000) A cortical area that responds specifically to optic flow, revealed by fMRI. Nat Neurosci 3(12):1322–1328. doi:10.1038/81860
Orban GA, Vanduffel W (2004) Functional mapping of motion regions. In: Werner LMCJS (ed) The visual neuroscience, vol 2. MIT Press, Cambridge, pp 1229–1246
Passarelli L, Rosa MG, Gamberini M, Bakola S, Burman KJ, Fattori P, Galletti C (2011) Cortical connections of area V6Av in the macaque: a visual-input node to the eye/hand coordination system. J Neurosci 31(5):1790–1801. doi:10.1523/JNEUROSCI.4784-10.2011
Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI (2006) Wide-field retinotopy defines human cortical visual area v6. J Neurosci 26(30):7962–7973. doi:10.1523/JNEUROSCI.0178-06.2006
Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Patria F, Galletti C (2010) Human v6: the medial motion area. Cereb Cortex 20(2):411–424. doi:10.1093/cercor/bhp112
Pitzalis S, Bozzacchi C, Bultrini A, Fattori P, Galletti C, Di Russo F (2013a) Parallel motion signals to the medial and lateral motion areas V6 and MT+. Neuroimage 67:89–100. doi:10.1016/j.neuroimage.2012.11.022
Pitzalis S, Fattori P, Galletti C (2013b) The functional role of the medial motion area V6. Front Behav Neurosci 6(91):1–13. doi:10.3389/fnbeh.2012.00091
Pitzalis S, Sdoia S, Bultrini A, Committeri G, Di Russo F, Fattori P, Galletti C, Galati G (2013c) Selectivity to translational egomotion in human brain motion areas. PLoS One 8(4):e60241. doi:10.1371/journal.pone.0060241PONE-D-12-38095
Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Tosoni A, Galletti C (2013d) The human homologue of macaque area V6A. NeuroImage 82:517–530
Power JD, Barnes KA, Snyder AZ, Schlagger BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154. doi:10.1016/j.neuroimage.2011.20.018
Power JD, Mitra A, Lauman TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84:320–341. doi:10.1016/j.neuroimage.2013.08.048
Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153(2):146–157. doi:10.1007/s00221-003-1588-0
Schluppeck D, Glimcher P, Heeger DJ (2005) Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol 94(2):1372–1384. doi:10.1152/jn.01290.2004
Sereno MI, Pitzalis S, Martinez A (2001) Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science 294(5545):1350–1354. doi:10.1126/science.1063695294/5545/1350
Shipp S, Zeki S (1989) The organization of connections between areas V5 and V1 in Macaque Monkey Visual Cortex. Eur J Neurosci 1(4):309–332 pii ejn_01040309
Silver MA, Ress D, Heeger DJ (2005) Topographic maps of visual spatial attention in human parietal cortex. J Neurophysiol 94(2):1358–1371. doi:10.1152/jn.01316.2004
Sulpizio V, Committeri G, Lambrey S, Berthoz A, Galati G (2013) Selective role of lingual/parahippocampal gyrus and retrosplenial complex in spatial memory across viewpoint changes relative to the environmental reference frame. Behav Brain Res 242:62–75. doi:10.1016/j.bbr.2012.12.031
Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27(20):5326–5337. doi:10.1523/JNEUROSCI.0991-07.2007
Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15(4):3215–3230
Tosoni A, Galati G, Romani GL, Corbetta M (2008) Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions. Nat Neurosci 11(12):1446–1453. doi:10.1038/nn.2221
Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, Menon V (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20(11):2636–2646. doi:10.1093/cercor/bhq011
Ungerleider LG, Mishkin M (1982) Two cortical visual system. Analysis of visual behavior. MIT, Cambridge
Van Essen DC, Glasser MF, Dierker DL, Harwell J, Coalson T (2011) Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. Cereb Cortex 22(10):2241–2262. doi:10.1093/cercor/bhr291
von Pfostl V, Stenbacka L, Vanni S, Parkkonen L, Galletti C, Fattori P (2009) Motion sensitivity of human V6: a magnetoencephalography study. Neuroimage 45(4):1253–1263. doi:10.1016/j.neuroimage.2008.12.058
Wall MB, Smith AT (2008) The representation of egomotion in the human brain. Curr Biol 18(3):191–194. doi:10.1016/j.cub.2007.12.053
Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zollei L, Polimeni JR, Fischl B, Liu H, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106(3):1125–1165. doi:10.1152/jn.00338.2011
Zeki S, Watson JD, Lueck CJ, Friston KJ, Kennard C, Frackowiak RS (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11(3):641–649
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This work was supported by RC block grants from Italian Ministry of Health—Fondazione Santa Lucia to GG and SP and by FP7-ICT-217077-EYESHOTS from MIUR and Fondazione del Monte di Bologna e Ravenna to CG.
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Tosoni, A., Pitzalis, S., Committeri, G. et al. Resting-state connectivity and functional specialization in human medial parieto-occipital cortex. Brain Struct Funct 220, 3307–3321 (2015). https://doi.org/10.1007/s00429-014-0858-x
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DOI: https://doi.org/10.1007/s00429-014-0858-x