Top

Published in:

01-08-2012 | Research Article

Interaction of cortical networks mediating object motion detection by moving observers

Authors: F. J. Calabro, L. M. Vaina

Published in: Experimental Brain Research | Issue 2/2012

Abstract

The task of parceling perceived visual motion into self- and object motion components is critical to safe and accurate visually guided navigation. In this paper, we used functional magnetic resonance imaging to determine the cortical areas functionally active in this task and the pattern connectivity among them to investigate the cortical regions of interest and networks that allow subjects to detect object motion separately from induced self-motion. Subjects were presented with nine textured objects during simulated forward self-motion and were asked to identify the target object, which had an additional, independent motion component toward or away from the observer. Cortical activation was distributed among occipital, intra-parietal and fronto-parietal areas. We performed a network analysis of connectivity data derived from partial correlation and multivariate Granger causality analyses among functionally active areas. This revealed four coarsely separated network clusters: bilateral V1 and V2; visually responsive occipito-temporal areas, including bilateral LO, V3A, KO (V3B) and hMT; bilateral VIP, DIPSM and right precuneus; and a cluster of higher, primarily left hemispheric regions, including the central sulcus, post-, pre- and sub-central sulci, pre-central gyrus, and FEF. We suggest that the visually responsive networks are involved in forming the representation of the visual stimulus, while the higher, left hemisphere cluster is involved in mediating the interpretation of the stimulus for action. Our main focus was on the relationships of activations during our task among the visually responsive areas. To determine the properties of the mechanism corresponding to the visual processing networks, we compared subjects’ psychophysical performance to a model of object motion detection based solely on relative motion among objects and found that it was inconsistent with observer performance. Our results support the use of scene context (e.g., eccentricity, depth) in the detection of object motion. We suggest that the cortical activation and visually responsive networks provide a potential substrate for this computation.

Available only for authorised users

Amedi A, Jacobson G, Hendler T, Malach R, Zohary E (2002) Convergence of visual and tactile shape processing in the human lateral occipital complex. Cereb Cortex 12:1202–1212PubMedCrossRef

Billington J, Field DT, Wilkie RM, Wann JP (2010) An fMRI study of parietal cortex involvement in the visual guidance of locomotion. J Exp Psychol Hum Percept Perform 36:1495–1507PubMedCrossRef

Brainard DH (1997) The psychophysics toolbox. Spatial Vis 10:433–436CrossRef

Bremmer F, Duhamel JR, Ben Hamed S, Graf W (1997) The representation of movement in near extrapersonal space in the macaque ventral intraparietal area (VIP). In: Thier P, Karnath HO (eds) Parietal Lobe Contributions to Orientation in 3D-Space. Springer, Heidelberg, pp 619–630

Bremmer F, Schlack A, Shah NJ et al (2001) Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29:287–296PubMedCrossRef

Burock MA, Dale AM (2000) Estimation and detection of event-related fMRI signals with temporally correlated noise: a statistically efficient and unbiased approach. Hum Brain Mapp 11:249–260PubMedCrossRef

Burock MA, Buckner RL, Woldorff MG, Rosen BR, Dale AM (1998) Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI. NeuroReport 9:3735–3739PubMedCrossRef

Calabro FJ, Soto-Faraco S, Vaina LM (2011) Acoustic facilitation of object movement detection during self-motion. Proceedings of the Royal Society of London B. 278:2840–2847CrossRef

Colby CL, Duhamel J-R, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902–914PubMed

Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194PubMedCrossRef

Duffy CJ, Wurtz RH (1991a) Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J Neurophysiol 65:1329–1345PubMed

Duffy CJ, Wurtz RH (1991b) Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. J Neurophysiol 65:1346–1359PubMed

Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136PubMed

Dupont P, De Bruyn B, Vandenberghe R et al (1997) The kinetic occipital region in human visual cortex. Cereb Cortex 7:283–292PubMedCrossRef

Durand JB, Peeters R, Norman JF, Todd JT, Orban GA (2009) Parietal regions processing visual 3D shape extracted from disparity. Neuroimage 46:1114–1126PubMedCrossRef

Eifuku S, Wurtz RH (1998) Response to motion in extrastriate area MSTl: center-surround interactions. J Neurophysiol 80:282–296PubMed

Eifuku S, Wurtz RH (1999) Response to motion in extrastriate area MSTl: disparity sensitivity. J Neurophysiol 82:2462–2475PubMed

Ffytche DH, Howseman A, Edwards R, Sandeman DR, Zeki S (2000) Human area V5 and motion in the ipsilateral visual field. Eur J Neurosci 12:3015–3025PubMedCrossRef

Field DT, Wann JP (2005) Perceiving time to collision activates the sensorimotor cortex. Curr Biol 15:453–458PubMedCrossRef

Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207PubMedCrossRef

Fischl B, Rajendran N, Busa E et al (2008) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973–1980PubMedCrossRef

Gilaie-Dotan S, Ullman S, Kushnir T, Malach R (2001) Shape-selective stereo processing in human object-related visual areas. Hum Brain Mapp 15:67–79CrossRef

Gogel WC (1990) A theory of phenomenal geometry and its applications. Percept Psychophys 48:105–123PubMedCrossRef

Granger CJW (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37:434–438

Green DM, Swets JA (1966) Signal detection theory and psychophysics. Wiley, New York

Heekeren HR, Marrett S, Bandettini PA, Ungerleider LG (2004) A general mechanism for perceptual decision-making in the human brain. Nature 431:859–862PubMedCrossRef

Hinds OP, Rajendran N, Polimeni JR et al (2008) Accurate prediction of V1 location from cortical folds in a surface coordinate system. Neuroimage 39:1585–1599PubMedCrossRef

Kaminski M, Ding M, Truccolo WA, Bressler SL (2001) Evaluating causal relations in neural systems: granger causality, directed transfer function and statistical assessment of significance. Biol Cybern 85:145–157PubMedCrossRef

Kayser AS, Buchsbaum BR, Erickson DT, D’Esposito M (2010) The functional anatomy of a perceptual decision in the human brain. J Neurophysiol 103:1179–1194PubMedCrossRef

Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital cortex. Science 293:1506–1509PubMedCrossRef

Leicht EA, Newman ME (2008) Community structure in directed networks. Phys Rev Lett 100:118703PubMedCrossRef

Malach R, Reppas JB, Benson RR et al (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92:8135–8139PubMedCrossRef

Mao L, Zhou B, Zhou W, Han S (2007) Neural correlates of covert orienting of visual spatial attention along vertical and horizontal dimensions. Brain Res 1136:142–153. doi:10.1016/j.brainres.2006.12.031 PubMedCrossRef

Matsumiya K, Ando H (2009) World-centered perception of 3D object motion during visually guided self-motion. Journal of Vision 9:1–13CrossRef

Mendola JD, Dale AM, Fischl B, Liu AK, Tootell RB (1999) The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging. The Journal of Neuroscience 19:8560–8572PubMed

Michels L, Lappe M, Vaina LM (2005) Visual areas involved in the perception of human movement from dynamic form analysis. NeuroReport 16:1037–1041PubMedCrossRef

Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577–8582PubMedCrossRef

Orban GA, Sunaert S, Todd JT, Hecke PV, Marchal G (1999) Human cortical regions involved in extracting depth from motion. Neuron 24:929–940PubMedCrossRef

Orban GA, Fize D, Peuskens H et al (2003) Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI. Neuropsychologia 41:1757–1768PubMedCrossRef

Pauwels K, Kruger N, Lappe M, Worgotter F, Van Hulle MM (2010) A cortical architecture on parallel hardware for motion processing in real time. J Vis 10:18PubMedCrossRef

Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spatial Vis 10:437–442CrossRef

Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25:230–242PubMedCrossRef

Royden CS, Connors EM (2010) The detection of moving objects by moving observers. Vision Res 50:1014–1024. doi:10.1016/j.visres.2010.03.008 PubMedCrossRef

Royden CS, Moore KD (2012) Use of speed cues in the detection of moving objects by moving observers. Vision Res 59:17–24. doi:10.1016/j.visres.2012.02.006 PubMedCrossRef

Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069PubMedCrossRef

Rushton SK, Duke PA (2007) The use of direction and distance information in the perception of approach trajectory. Vision Res 47:899–912PubMedCrossRef

Rushton SK, Warren PA (2005) Moving observers, relative retinal motion and the detection of object movement. Curr Biol 15:R542–R543PubMedCrossRef

Seth AK (2010) A MATLAB toolbox for Granger causal connectivity analysis. J Neurosci Methods 186:262–273PubMedCrossRef

Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J (1998) The processing of first- and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). J Neurosci 18:3816–3830PubMed

Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219PubMedCrossRef

Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127:355–370PubMedCrossRef

Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, New York

Tanaka K, Saito H (1989) Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. J Neurophysiol 62:626–641PubMed

Tanaka K, Sugita Y, Moriya M, Saito H (1993) Analysis of object motion in the ventral part of the medial superior temporal area of the macaque visual cortex. J Neurophysiol 69:128–142PubMed

Tootell RBH, Kwong KK, Belliveau JW et al (1993) Functional MRI (fMRI) evidence for MT/V5 and associated visual cortical areas in man. In: Society for Neuroscience 23rd annual meeting, vol 19. Society for neuroscience, Washington DC, p 1500

Tootell RBH, Reppas JB, Kwong KK et al (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neuroscience 15(4):3215–3230

Tootell RB, Mendola JD, Hadjikhani NK et al (1997) Functional analysis of V3a and related areas in human visual cortex. J Neurosci 17:7060–7078PubMed

Tyler CW, Likova LT, Kontsevich LL, Wade AR (2006) The specificity of cortical region KO to depth structure. Neuroimage 30:228–238PubMedCrossRef

Vaina LM, Soloviev S (2004) Functional neuroanatomy of self-motion perception in humans. In: Vaina LM, Beardsley SA, Rushton S (eds) Optic flow and beyond. Kluwer, Dordrecht, pp 109–137

Vaina LM, Belliveau JW, des Roziers EB, Zeffiro TA (1998) Neural systems underlying learning and representation of global motion. Proc Nat Acad Sci USA 95:12657–12662PubMedCrossRef

Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW (2001) Functional neuroanatomy of biological motion perception in humans. Proc Natl Acad Sci USA 98:11656–11661PubMedCrossRef

Vaina L, Calabro F, Lin F, Hamalainen M (2010a) Long-range coupling of prefrontal cortex and visual (MT) or polysensory (STP) cortical areas in motion perception. BIOMAG2010, IFBME Proc, Springer,IFBME 28:298–301

Vaina LM, Sikoglu EM, Soloviev S, Lemay M, Squatrito S, Pandiani G, Cowey A (2010b) Functional and anatomical profile of visual motion impairments in stroke patients correlate with fMRI in normal subjects. J Neuropsychol 4:121–145 (PMCID:PMC2935516)PubMedCrossRef

van der Kouwe AJ, Benner T, Fischl B et al (2005) On-line automatic slice positioning for brain MR imaging. Neuroimage 27:222–230PubMedCrossRef

Van Oostende S, Sunaert S, Van Hecke P, Marchal G, Orban GA (1997) The kinetic occipital (KO) region in man: an fMRI study. Cereb Cortex 7:690–701PubMedCrossRef

Wallach H (1987) Perceiving a stable environment when one moves. Annu Rev Psychol 38:1–27PubMedCrossRef

Warren PA, Rushton SK (2007) Perception of object trajectory: parsing retinal motion into self and object movement components. J Vis 7(2):1–11PubMedCrossRef

Warren PA, Rushton SK (2009) Perception of scene-relative object movement: optic flow parsing and the contribution of monocular depth cues. Vision Res 49:1406–1419PubMedCrossRef

Title: Interaction of cortical networks mediating object motion detection by moving observers
Authors: F. J. Calabro
L. M. Vaina
Publication date: 01-08-2012
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 2/2012
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-012-3159-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Interaction of cortical networks mediating object motion detection by moving observers

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2012

Force and time gain interact to nonlinearly scale adaptive visual-motor isometric force control

Oral hapsis guides accurate hand preshaping for grasping food targets in the mouth

Ankle joint movements are encoded by both cutaneous and muscle afferents in humans

Proprioceptive reaction times and long-latency reflexes in humans

Perceptual learning in temporal discrimination: asymmetric cross-modal transfer from audition to vision

Alpha oscillations and the control of voluntary saccadic behavior