JBBS  Vol.3 No.1 , February 2013
Study of the Neural Basis for Subjective Feature Binding
Abstract: While it is known that the brain perceives color and motion asynchronously, the specific locations in which the brain binds signals remain unknown. This study distinguishes subjective perception of the capability to bind features and the objective accuracy in feature binding. The stimuli were the same for individual subjects, consisting of random dots (red and green, or yellow and blue) moving either vertically or horizontally. Subjects responded to questions regarding the color or the direction of motion of the dots (objective judgment) and rated their capability in performing the task (subjective judgment). The imaging results of contrasting subjective judgment showed that the activation of the anterior rostral cingulate cortex (rACC) and inferior frontal gyrus (Brodmann area [BA] 45/47) during incapable-of-binding responses, compared with the capable-of-binding responses. It is suggested that the rACC is for uncertainty of subjective judgment and BA 45/47 is for the increased burden on working memory. In contrast, there was no imaging results of contrasting the correct and incorrect responses (i.e., objective judgment), and neither was there for the interaction between subjective and objective judgment. The results of conservative conjunction analysis indicated common and shared brain areas for the 2 distinctive binding situations (the correct and capable-of-binding vs the incorrect and incapable-of-binding), including increased activity in the intraparietal lobe (IPL) and the junction areas of the posterior rostral ACC (dACC) and the prefrontal areas, but decreased activity in the medial portion of the IPL, suggesting that feature binding requires maintaining attention. These results clearly isolated subjective judgment from objective judgment and support the view that maintaining attention is involved in feature binding of color and motion.
Cite this paper: T. Chiang, J. Chen, K. Liang, C. Cheng, S. Hsiao, C. Hsieh, Y. Huang and C. Li, "Study of the Neural Basis for Subjective Feature Binding," Journal of Behavioral and Brain Science, Vol. 3 No. 1, 2013, pp. 57-66. doi: 10.4236/jbbs.2013.31006.

[1]   M. Livingstone and D. Hubel, “Segregation of Form, Color, Movement, and Depth: Anatomy, Physiology, and Perception,” Science, Vol. 240, No. 4853, 1988, pp. 740749. doi:10.1126/science.3283936

[2]   S. Zeki, “Functional Specialisation in the Visual Cortex of the Rhesus Monkey,” Nature, Vol. 274, No. 5670, 1978, pp. 423-428. doi:10.1038/274423a0

[3]   K. Moutoussis and S. Zeki, “A Direct Demonstration of Perceptual Asynchrony in Vision,” Proceedings of Biological Sciences, Vol. 264, No. 1380, 1997, pp. 393-399. doi:10.1098/rspb.1997.0056

[4]   A. Treisman, “The Binding Problem,” Current Opinion in Neurobiology, Vol. 6, No. 2, 1996, pp. 171-178. doi:10.1016/S0959-4388(96)80070-5

[5]   E. Ashbridge, V. Walsh and A. Cowey, “Temporal Aspects of Visual Search Studied by Transcranial Magnetic Stimulation,” Neuropsychologia, Vol. 35, No. 8, 1997, pp. 1121-1131. doi:10.1016/S0028-3932(97)00003-1

[6]   M. Corbetta, et al., “Superior Parietal Cortex Activation during Spatial Attention Shifts and Visual Feature Conjunction,” Science, Vol. 270, No. 5237, 1995, pp. 802805. doi:10.1126/science.270.5237.802

[7]   M. Corbetta, C. M. Sylvester and G. L. HShulman, “The Frontoparietal Attention Network,” In: The Cognitive Neurosciences, MIT Press, Cambridge, 2009, pp. 219-233.

[8]   S. R. Friedman-Hill, L. C. Robertson and A. Treisman, “Parietal Contributions to Visual Feature Binding: Evidence from a Patient with Bilateral Lesions,” Science, Vol. 269, No. 5225, 1995, pp. 853-835. doi:10.1126/science.7638604

[9]   S. Kastner, S. A. McMains and D. Beck, “Mechanisms of Selective Attention in the Human Visual System: Evidence from Neuroimaging,” In: The Cognitive Neurosciences, MIT Press, Cambridge, 2009, pp. 205-217.

[10]   M. Oliveri, et al., “Facilitation of Bottom-Up Feature Detection Following rTMS-Interference of the Right Parietal Cortex,” Neuropsychologia, Vol. 48, No. 4, 2010, pp. 1003-1010. doi:10.1016/j.neuropsychologia.2009.11.024

[11]   A. Treisman and G. Gelade, “A Feature-Integration Theory of Attention,” Cognitive Psychology, Vol. 12, No. 1, 1980, pp. 97-136. doi:10.1016/0010-0285(80)90005-5

[12]   S. M. Fleming and R. J. Dolan, “The Neural Basis of Metacognitive Ability,” Philosophical Transactions of the Royal Society B-Biological Sciences, Vol. 367, No. 1594, 2012, pp. 1338-1349. doi:10.1098/rstb.2011.0417

[13]   H. C. Lau and R. E. Passingham, “Relative Blindsight in Normal Observers and the Neural Correlate of Visual Consciousness,” Proceedings of the National Academy of Sciences, Vol. 103, No. 49, 2006, pp. 18763-18768. doi:10.1073/pnas.0607716103

[14]   D. Rosenthal, “Higher-Order Awareness, Misrepresentation and Function,” Philosophical Transactions of the Royal Society B-Biological Sciences, Vol. 367, No. 1594, 2012, pp. 1424-1438. doi:10.1098/rstb.2011.0353

[15]   P. K. Kaiser, “Flicker as a Function of Wavelength and Heterochromatic Flicker Photometry,” In: Vision and Dysfunction, Basingstoke, MacMilliap, 1991, pp. 171-190.

[16]   N. E. Breslow and D. G. Clayton, “Approximate Inference in Generalized Linear Mixed Models,” Journal of Computational and Graphical Statistics, Vol. 88, No. 421, 1993, pp. 9-25.

[17]   T. F. Jaeger, “Categorical Data Analysis: Away from ANOVAs (Transformation or Not) and towards Logit Mixed Models,” Journal of Memory and Language, Vol. 59, No. 4, 2008, pp. 434-446. doi:10.1016/j.jml.2007.11.007

[18]   K. J. Friston, W. D. Penny and D. E. Glaser, “Conjunction Revisited,” Neuroimage, Vol. 25, No. 3, 2005, pp. 661-667. doi:10.1016/j.neuroimage.2005.01.013

[19]   T. Nichols, et al., “Valid Conjunction Inference with the Minimum Statistic,” Neuroimage, Vol. 25, No. 3, 2005, pp. 653-660. doi:10.1016/j.neuroimage.2004.12.005

[20]   Z. Dienes, “Subjective Measures of Unconscious Knowledge,” Progress in Brain Research, Vol. 168, 2007, pp. 49-64.

[21]   H. C. Lau and R. E. Passingham, “Unconscious Activation of the Cognitive Control System in the Human Prefrontal Cortex,” Journal of Neuroscience, Vol. 27, No. 21, 2007, pp. 5805-5811. doi:10.1523/JNEUROSCI.4335-06.2007

[22]   A. Sahraie, et al., “Pattern of Neuronal Activity Associated with Conscious and Unconscious Processing of Visual Signals,” Proceedings of the National Academy of Sciences, Vol. 94, No. 17, 1997, pp. 9406-9411. doi:10.1073/pnas.94.17.9406

[23]   M. M. Botvinick, “Conflict Monitoring and Decision Making: Reconciling Two Perspectives on Anterior Cingulate Function,” Cognitive, Affective, & Behavioral Neuroscience, Vol. 7, No. 4, 2007, pp. 356-366. doi:10.3758/CABN.7.4.356

[24]   M. F. Rushworth and T. E. Behrens, “Choice, Uncertainty and Value in Prefrontal and Cingulate Cortex,” Nature Neuroscience, Vol. 11, No. 4, 2008, pp. 389-397. doi:10.1038/nn2066

[25]   J. W. Brown and T. S. Braver, “Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex,” Science, Vol. 307, No. 5712, 2005, pp. 1118-1121. doi:10.1126/science.1105783

[26]   H. Ohira, et al., “Brain and Autonomic Association Accompanying Stochastic Decision-Making,” Neuroimage, Vol. 49, No. 1, 2010, pp. 1024-1037. doi:10.1016/j.neuroimage.2009.07.060

[27]   M. H. Davis, et al., “Dissociating Speech Perception and Comprehension at Reduced Levels of Awareness,” Proceedings of the National Academy of Sciences, Vol. 104, No. 41, 2007, pp. 16032-16037. doi:10.1073/pnas.0701309104

[28]   K. Hoenig and L. Scheef, “Mediotemporal Contributions to Semantic Processing: fMRI Evidence from Ambiguity Processing during Semantic Context Verification,” Hippocampus, Vol. 15, No. 5, 2005, pp. 597-609. doi:10.1002/hipo.20080

[29]   J. M. Rodd, M. H. Davis and I. S. Johnsrude, “The Neural Mechanisms of Speech Comprehension: fMRI Studies of Semantic Ambiguity,” Cereb Cortex, Vol. 15, No. 8, 2005, pp. 1261-1269. doi:10.1093/cercor/bhi009

[30]   M. Z. Zempleni, et al., “Semantic Ambiguity Processing in Sentence Context: Evidence from Event-Related fMRI,” Neuroimage, Vol. 34, No. 3, 2007, pp. 1270-1279. doi:10.1016/j.neuroimage.2006.09.048

[31]   A. F. Hamilton and S. T. Grafton, “Action Outcomes Are Represented in Human Inferior Frontoparietal Cortex,” Cereb Cortex, Vol. 18, No. 5, 2008, pp. 1160-1168. doi:10.1093/cercor/bhm150

[32]   M. Iacoboni, et al., “Grasping the Intentions of Others with One’s Own Mirror Neuron System,” PLoS Biology, Vol. 3, No. 3, 2005, p. e79. doi:10.1371/journal.pbio.0030079

[33]   G. Rizzolati, L. Fogassi and V. Gallese, “The Mirror Neuron System: A Motor-Based Mechanism for Action and Intention Understanding,” In: The Cognitive Neuroscience, The MIT Press, Cambridge, 2009, pp. 625-640.

[34]   N. Gorgoraptis, et al., “Dynamic Updating of Working Memory Resources for Visual Objects,” Journal of Neuroscience, Vol. 31, No. 23, 2011, pp. 8502-8511. doi:10.1523/JNEUROSCI.0208-11.2011

[35]   S. Takahama, S. Miyauchi and J. Saiki, “Neural Basis for Dynamic Updating of Object Representation in Visual Working Memory,” Neuroimage, Vol. 49, No. 4, 2010, pp. 3394-3403. doi:10.1016/j.neuroimage.2009.11.029

[36]   X. Li, et al., “Blood Oxygenation Level-Dependent Contrast Response Functions Identify Mechanisms of Covert Attention in Early Visual Areas,” Proceedings of the National Academy of Sciences, Vol. 105, No. 16, 2008, pp. 6202-6207. doi:10.1073/pnas.0801390105

[37]   Z. L. Lu, et al., “Attention Extracts Signal in External Noise: A Bold fMRI Study,” Journal of Cognitive Neuroscience, Vol. 23, No. 5, 2011, pp. 1148-1159. doi:10.1162/jocn.2010.21511

[38]   A. G. Leventhal, et al., “Concomitant Sensitivity to Orientation, Direction, and Color of Cells in Layers 2, 3, and 4 of Monkey Striate Cortex,” Journal of Neuroscience, Vol. 15, No. 3, 1995, pp. 1808-1818.

[39]   E. Blaser, T. Papathomas and Z. Vidnyanszky, “Binding of Motion and Colour Is Early and Automatic,” European Journal of Neuroscience, Vol. 21, No. 7, 2005, pp. 20402044. doi:10.1111/j.1460-9568.2005.04032.x

[40]   A. O. Holcombe and P. Cavanagh, “Early Binding of Feature Pairs for Visual Perception,” Nature Neuroscience, Vol. 4, No. 2, 2001, pp. 127-128. doi:10.1038/83945

[41]   K. Seymour, et al., “The Coding of Color, Motion, and Their Conjunction in the Human Visual Cortex,” Current Biology, Vol. 19, No. 3, 2009, pp. 177-183. doi:10.1016/j.cub.2008.12.050

[42]   O. J. Hulme, L. Whiteley and S. Shipp, “Spatially Distributed Encoding of Covert Attentional Shifts in Human Thalamus,” Journal of Neurophysiology, Vol. 104, No. 6, 2010, pp. 3644-3656.

[43]   S. Shipp, et al., “Feature Binding in the Feedback Layers of Area V2,” Cereb Cortex, Vol. 19, No. 10, 2009, pp. 2230-2239. doi:10.1093/cercor/bhn243

[44]   A. Treisman and H. Schmidt, “Illusory Conjunctions in the Perception of Objects,” Cognitive Psychology, Vol. 14, No. 1, 1982, pp. 107-141. doi:10.1016/0010-0285(82)90006-8

[45]   R. Ward, et al., “Deficits in Spatial Coding and Feature Binding Following Damage to Spatiotopic Maps in the Human Pulvinar,” Nature Neuroscience, Vol. 5, No. 2, 2002, pp. 99-100.

[46]   G. Wolford and K. H. Shum, “Evidence for Feature Perturbations,” Percept Psychophys, Vol. 27, No. 5, 1980, pp. 409-420. doi:10.3758/BF03204459

[47]   C. Casanova, “The Visual Functions of the Pulvinar,” In: The Visual Neurosciences, MIT Press, Cambridge, 2004.

[48]   S. Kastner and M. A. Pinsk, “Visual Attention as a Multilevel Selection Process,” Cognitive, Affective, & Behavioral Neuroscience, Vol. 4, No. 4, 2004, pp. 483-500. doi:10.3758/CABN.4.4.483

[49]   M. Corbetta and G. L. Shulman, “Control of Goal-Directed and Stimulus-Driven Attention in the Brain,” Nature Reviews Neuroscience, Vol. 3, 2002, pp. 201-215.

[50]   J. Hopfinger, M. H. Buonocore and G. R. Mangun, “The Neural Mechanisms of Top-Down Attentional Control,” Nature Neuroscience, Vol. 3, 2000, pp. 284-291.

[51]   S. Kastner, et al., “Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation,” Neuron, Vol. 22, No. 4, 1999, pp. 751761. doi:10.1016/S0896-6273(00)80734-5

[52]   T. Liu, et al., “Cortical Mechanisms of Feature-Based Attentional Control,” Cereb Cortex, Vol. 13, 2003, pp. 1334-1343.

[53]   T. A. Kelley, et al., “Cortical Mechanisms for Shifting and Holding Visuospatial Attention,” Cereb Cortex, Vol. 18, No. 1, 2008, pp. 114-125. doi:10.1093/cercor/bhm036

[54]   J. T. Serences and S. Yantis, “Spatially Selective Representations of Voluntary and Stimulus-Driven Attentional Priority in Human Occipital, Parietal, and Frontal Cortex,” Cereb Cortex, Vol. 17, No. 2, 2007, pp. 284-293. doi:10.1093/cercor/bhj146

[55]   R. Vandenberghe, et al., “Functional Specificity of Superior Parietal Mediation of Spatial Shifting,” Neuroimage, Vol. 14, 2001, pp. 661-673.

[56]   L. Huang, A. Treisman and H. Pashler, “Characterizing the Limits of Human Visual Awareness,” Science, Vol. 317, No. 5839, 2007, pp. 823-825. doi:10.1126/science.1143515

[57]   L. Huang and H. Pashler, “A Boolean Map Theory of Visual Attention,” Psychological Review, Vol. 114, 2007, pp. 599-631.

[58]   L. Huang, “What Is the Unit of Visual Attention? Object for Selection, but Boolean Map for Access,” Journal of Experimental Psychology: General, Vol. 139, 2010, pp. 162-179