All Title Author
Keywords Abstract

PLOS ONE  2007 

A Functional Architecture of Optic Flow in the Inferior Parietal Lobule of the Behaving Monkey

DOI: 10.1371/journal.pone.0000200

Full-Text   Cite this paper   Add to My Lib

Abstract:

The representation of navigational optic flow across the inferior parietal lobule was assessed using optical imaging of intrinsic signals in behaving monkeys. The exposed cortex, corresponding to the dorsal-most portion of areas 7a and dorsal prelunate (DP), was imaged in two hemispheres of two rhesus monkeys. The monkeys actively attended to changes in motion stimuli while fixating. Radial expansion and contraction, and rotation clockwise and counter-clockwise optic flow stimuli were presented concentric to the fixation point at two angles of gaze to assess the interrelationship between the eye position and optic flow signal. The cortical response depended upon the type of flow and was modulated by eye position. The optic flow selectivity was embedded in a patchy architecture within the gain field architecture. All four optic flow stimuli tested were represented in areas 7a and DP. The location of the patches varied across days. However the spatial periodicity of the patches remained constant across days at ~950 and 1100 μm for the two animals examined. These optical recordings agree with previous electrophysiological studies of area 7a, and provide new evidence for flow selectivity in DP and a fine scale description of its cortical topography. That the functional architectures for optic flow can change over time was unexpected. These and earlier results also from inferior parietal lobule support the inclusion of both static and dynamic functional architectures that define association cortical areas and ultimately support complex cognitive function.

References

[1]  Raffi M, Siegel RM (2004) Multiple cortical representation of optic flow processing. In: Vaina LM, Beardsley SA, Rushton SK, editors. “Optic flow and beyond”. Kluwer. pp. 3–22.
[2]  Critchley M (1953) New York. The parietal lobes; press H, editor.
[3]  Andersen RA (1989) Visual and eye movement functions of the posterior parietal cortex. Annu Rev Neurosci 12: 377–403.
[4]  Read HL, Siegel RM (1997) Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkeys. Cereb Cortex 7: 647–661.
[5]  Raffi M, Siegel RM (2005) Functional architecture of spatial attention in the parietal cortex of the behaving monkey. J Neurosci 25: 5171–5186.
[6]  Vaina LM, Gryzwac N, Bienfang D (1994) Selective deficits of motion integration and segregation mechanisms with unilateral extrastriate brain lesions. Invest Ophtalomol Vis Sci 35: 1438.
[7]  Vaina LM, Rushton SK (2000) What neurological patients tell us about the use of optic flow. In: Lappe M, editor. International review of neurobiology. San Diego: Academic Press. pp. 293–313.
[8]  Siegel RM, Read HL (1997) Analysis of optic flow in the monkey parietal area 7a. Cereb Cortex 7: 327–346.
[9]  Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38: 871–908.
[10]  Li C, Tanaka M, Creutzfeldt OD (1989) Attention and eye movement related activation of neurons in the dorsal prelunate gyrus (area DP). Brain Res 496: 307–313.
[11]  Constantinidis C, Steinmetz MA (2001) Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location. Cereb Cortex 11: 592–597.
[12]  Constantinidis C, Steinmetz MA (2001) Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus. Cereb Cortex 11: 581–591.
[13]  Bushnell MC, Goldberg ME, Robinson DL (1981) Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. J Neurophysiol 46: 755–772.
[14]  Siegel RM, Raffi M, Phinney RE, Turner JA, Jando G (2003) Functional architecture of eye position gain fields in visual association cortex of behaving monkey. J Neurophysiol 90: 1279–1294.
[15]  Heider B, Jando G, Siegel RM (2005) Functional architecture of retinotopy in visual association cortex of behaving monkey. Cereb Cortex 15: 460–478.
[16]  Arieli A, Grinvald A (2002) Optical imaging combined with targeted electrical recordings, microstimulation, or tracer injections. J Neurosci Methods 116: 15–28.
[17]  Shtoyerman E, Arieli A, Slovin H, Vanzetta I, Grinvald A (2000) Long-term optical imaging and spectroscopy reveal mechanisms underlying the intrinsic signal and stability of cortical maps in V1 of behaving monkeys. J Neurosci 20: 8111–8121.
[18]  Anderson KC, Siegel RM (1999) Optic flow selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey. J Neurosci 19: 2681–2692.
[19]  Merchant H, Battaglia-Mayer A, Georgopoulos AP (2001) Effects of optic flow in motor cortex and area 7a. J Neurophysiol 86: 1937–1954.
[20]  Merchant H, Battaglia-Mayer A, Georgopoulos AP (2003) Functional organization of parietal neuronal responses to optic-flow stimuli. J Neurophysiol 90: 675–682.
[21]  Steinmetz MA, Motter BC, Duffy CJ, Mountcastle VB (1987) Functional properties of parietal visual neurons: radial organization of directionalities within the visual field. JNeurosci 7: 177–191.
[22]  Motter BC, Steinmetz MA, Duffy CJ, Mountcastle VB (1987) Functional properties of parietal visual neurons: mechanisms of directionality along a single axis. JNeurosci 7: 154–176.
[23]  Siegel RM, Andersen RA (1988) Perception of three-dimensional structure from two-dimensional motion in monkey and man. Nature 331: 259–261.
[24]  Batschelet E (1981) Circular statistics in biology;. In: Sibson R, Cohen JE, editors. London and New York: Academic Press.
[25]  Graziano MSA, Andersen RA, Snowden RJ (1994) Tuning of MST neurons to spiral motion. J Neurosci 14: 56–67.
[26]  Phinney RE, Siegel RM (1996) Behavioral modulation of speed tuning for neurons in area 7a in the behaving macaque. AbstrSocNeurosci 22: 1693.
[27]  Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87: 6082–6086.
[28]  Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN (1986) Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324: 361–364.
[29]  Siegel RM, Duann JR, Jung TP, Sejnowski T (2006) Spatiotemporal Dynamics of the Functional Architecture for Gain Fields in Inferior Parietal Lobule of Behaving Monkey. Cereb Cortex.
[30]  Duann JR, Jung TP, Kuo WJ, Yeh TC, Makeig S, et al. (2002) Single-trial variability in event-related BOLD signals. Neuroimage 15: 823–835.
[31]  Malonek D, Dirnagl U, Lindauer U, Yamada K, Kanno I, et al. (1997) Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc Natl Acad Sci USA 94: 14826–14831.
[32]  Longuet-Higgins HC, Prazdny K (1980) The interpretation of a moving retinal image. ProcRoySocLondB 208: 385–397.
[33]  Ullman S (1979) The interpretation of structure from motion. ProcRSocLondBiol 203: 405–426.
[34]  Marr D (1982) Vision. San Francisco: W.H. Freeman and Co.
[35]  Perrone JA, Stone LS (1994) A model of self-motion estimation within primate extrastriate visual cortex. Vision Research 34: 2917–2938.
[36]  Duffy CJ, Wurtz RH (1991) Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J Neurophysiol 65: 1345–1345.
[37]  Britten KH, Van Wezel RJ (2002) Area MST and heading perception in macaque monkeys. Cereb Cortex 12: 692–701.
[38]  Siegel RM, Andersen RA (1990) The perception of structure from motion in monkey and man. JCognitive Neurosci 2: 306–319.
[39]  Lagae L, Maes H, Raiguel S, Xiao DK, Orban GA (1994) Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. JNeurophys 71: 1597–1626.
[40]  Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. JNeurophys 46: 369–384.
[41]  Duffy CJ, Wurtz RH (1991) Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. JNeurophys 65: 1346–1359.
[42]  Tanaka K, Hikosaka K, Saito H, Yukie M, Fukada Y, et al. (1986) Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. JNeurosci 6: 134–144.
[43]  Andersen RA, Asanuma C, Essick G, Siegel RM (1990) Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J Comp Neurol 296: 65–113.
[44]  Pigarev IN, Nothdurft HC, Kastner S (2001) Neurons with large bilateral receptive fields in monkey prelunate gyrus. Exp Brain Res 136: 108–113.
[45]  Maguire WM, Baizer JS (1984) Visuotopic organization of the prelunate gyrus in the rhesus monkey. J Neurosci 4: 1690–1704.
[46]  Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol 287: 393–421.
[47]  Geesaman BJ, Born RT, Andersen RA, Tootell RB (1997) Maps of complex motion selectivity in the superior temporal cortex of the alert macaque monkey: a double-label 2-deoxyglucose study. Cereb Cortex 7: 749–757.
[48]  Britten KH (1998) Clustering of response selectivity in the medial superior temporal area of extrastriate cortex in the macaque monkey. Vis Neurosci 15: 553–558.
[49]  Britten KH, van Wezel RJ (1998) Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat Neurosci 1: 59–63.
[50]  Stettler DD, Das A, Bennett J, Gilbert CD (2002) Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36: 739–750.
[51]  Siegel RM, Read HL (1997) Construction and representation of visual space in the inferior parietal lobule. In: Kaas J, Rockland K, Peters A, editors. Cerebral Cortex. New York: Plenum. pp. 499–525.
[52]  Arnsten AF, Goldman-Rakic PS (1984) Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus monkey. Brain Res 306: 9–18.
[53]  Golmayo L, Nunez A, Zaborszky L (2003) Electrophysiological evidence for the existence of a posterior cortical-prefrontal-basal forebrain circuitry in modulating sensory responses in visual and somatosensory rat cortical areas. Neuroscience 119: 597–609.
[54]  Cavada C, Goldman-Rakic PS (1991) Topographic segregation of corticostriatal projections from posterior parietal subdivisions in the macaque monkey. Neuroscience 42: 683–696.
[55]  Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, et al. (1990) Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248: 229–231.
[56]  Darian-Smith C, Gilbert CD (1995) Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J Neurosci 15: 1631–1647.
[57]  Jenkins WM, Merzenich MM, Ochs MT, Allard T, Guic-Robles E (1990) Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J Neurophysiol 63: 82–104.
[58]  Cossart R, Aronov D, Yuste R (2003) Attractor dynamics of network UP states in the neocortex. Nature 423: 283–288.
[59]  Polley DB, Chen-Bee CH, Frostig RD (1999) Two directions of plasticity in the sensory-deprived adult cortex. Neuron 24: 623–637.
[60]  Crick F, Koch C (2003) A framework for consciousness. Nat Neurosci 6: 119–126.
[61]  Sporns , Gally JA, Reeke GN, Edelman GM (1989) Reentrant signaling among simulated neuronal groups lead to coherency in their oscillatory activity. ProcNatlAcadSciUSA 86: 7265–7269.
[62]  Karni A, Meyer G, Jezzard P, Adams MM, Turner R, et al. (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377: 155–158.
[63]  Birbaumer N, Lutzenberger W, Montoya P, Larbig W, Unertl K, et al. (1997) Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization. J Neurosci 17: 5503–5508.
[64]  Spengler F, Roberts TP, Poeppel D, Byl N, Wang X, et al. (1997) Learning transfer and neuronal plasticity in humans trained in tactile discrimination. Neurosci Lett 232: 151–154.
[65]  Buchner H, Reinartz U, Waberski TD, Gobbele R, Noppeney U, et al. (1999) Sustained attention modulates the immediate effect of de-afferentation on the cortical representation of the digits: source localization of somatosensory evoked potentials in humans. Neurosci Lett 260: 57–60.
[66]  Menning H, Roberts LE, Pantev C (2000) Plastic changes in the auditory cortex induced by intensive frequency discrimination training. Neuroreport 11: 817–822.
[67]  Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, et al. (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci U S A 97: 3661–3665.
[68]  Rossini PM, Pauri F (2000) Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas ‘plastic’ reorganisation. Brain Res Brain Res Rev 33: 131–154.
[69]  Van Essen DC (1985) Functional organization of primate visual cortex. In: Peters A, Jones EG, editors. Cerebral cortex: visual cortex. New York and London: Plenum press. pp. 259–329.
[70]  Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287: 422–445.
[71]  Andersen RA, Asanuma C, Cowan WM (1985) Callosal and prefrontal projecting cell populations in area 7a of the macaque monkey: a study using retrogradely transported fluorescent dyes. J Comp Neurol 232: 443–455.
[72]  Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352: 161–186.
[73]  Kondo H, Tanaka K, Hashikawa T, Jones EG (1999) Neurochemical gradients along monkey sensory cortical pathways: calbindin-immunoreactive pyramidal neurons in layers II and III. Eur J Neurosci 11: 4197–4203.
[74]  Kleinfeld D, Griesbeck O (2005) From art to engineering? The rise of in vivo mammalian electrophysiology via genetically targeted labeling and nonlinear imaging. PLoS Biol 3: e355.
[75]  Crick FH (1979) Thinking about the brain. Sci Am 241: 219–232.

Full-Text

comments powered by Disqus

Contact Us

service@oalib.com

QQ:3279437679

微信:OALib Journal