Is that a belt or a snake? object attentional selection affects the early stages of visual sensory processing

Behavioral and Brain Functions

Alberto Zani²  Alice M Proverbio¹ 

[1] Department of Psychology, University of Milano-Bicocca, Milan, Italy

[2] Electro-Functional Brain Imaging unit (EFBIu), Institute of Molecular Bioimaging and Physiology, CNR, Milan, Italy

关键词: shape categorization;    shape processing time course;    space and object parallel processing;    V1;    visual striate cortex;    visual selective attention;    N1;    P1;    C1;    ERPs;   

Others  :  797557
DOI  :  10.1186/1744-9081-8-6

 received in 2011-05-31, accepted in 2012-02-02,  发布年份 2012

【 摘 要 】

Background

There is at present crescent empirical evidence deriving from different lines of ERPs research that, unlike previously observed, the earliest sensory visual response, known as C1 component or P/N80, generated within the striate cortex, might be modulated by selective attention to visual stimulus features. Up to now, evidence of this modulation has been related to space location, and simple features such as spatial frequency, luminance, and texture. Additionally, neurophysiological conditions, such as emotion, vigilance, the reflexive or voluntary nature of input attentional selection, and workload have also been related to C1 modulations, although at least the workload status has received controversial indications. No information is instead available, at present, for objects attentional selection.

Methods

In this study object- and space-based attention mechanisms were conjointly investigated by presenting complex, familiar shapes of artefacts and animals, intermixed with distracters, in different tasks requiring the selection of a relevant target-category within a relevant spatial location, while ignoring the other shape categories within this location, and, overall, all the categories at an irrelevant location. EEG was recorded from 30 scalp electrode sites in 21 right-handed participants.

Results and Conclusions

ERP findings showed that visual processing was modulated by both shape- and location-relevance per se, beginning separately at the latency of the early phase of a precocious negativity (60-80 ms) at mesial scalp sites consistent with the C1 component, and a positivity at more lateral sites. The data also showed that the attentional modulation progressed conjointly at the latency of the subsequent P1 (100-120 ms) and N1 (120-180 ms), as well as later-latency components. These findings support the views that (1) V1 may be precociously modulated by direct top-down influences, and participates to object, besides simple features, attentional selection; (2) object spatial and non-spatial features selection might begin with an early, parallel detection of a target object in the visual field, followed by the progressive focusing of spatial attention onto the location of an actual target for its identification, somehow in line with neural mechanisms reported in the literature as "object-based space selection", or with those proposed for visual search.

【 授权许可】

   
2012 Zani and Proverbio; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Martínez A, Anllo-Vento L, Sereno MI, Frank LR, Buxton RB, Dubowitz DJ, Wong EC, Hinrichs H, Heinze HJ, Sa H: Involvement of striate and extrastriate visual cortical areas in spatial attention. Nature Neurosci 1999, 2:364-369.
• [2]Martínez A, Di Russo F, Anllo-Vento L, Sereno MI, Buxton RB, Hillyard SA, H : Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res 2001, 41:1537-1547.
• [3]Baas JM, Kenemans JL: Selective attention to spatial frequency: an ERP and source localization analysis. Clin Neurophysiol 2002, 13:1840-1854.
• [4]Hillyard SA, Anllo-Vento L: Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci USA 1998, 95:781.
• [5]Grunewald A, Bradley DC, Andersen RA: Neural Correlates of Structure form-Motion Perception in Macaque V1 and MT. J Neurosci 2002, 22:6195-6207.
• [6]Luck SJ, Chelazzi L, Hillyard SA, Desimone R: Neural Mechanisms of Spatial Selective Attention in Areas V1, V2, and V4 of Macaque Visual Cortex. J Neurophysiol 1997, 77:24-42.
• [7]Aine CJ, Supek S, George JS: Temporal dynamics of visual-evoked neuromagnetic sources: effects of stimulus parameters and selective attention. The Internat J Neurosci 1995, 80:79-104.
• [8]Treue S: Neural correlates of attention in primate visual cortex. Trends Neurosci 2001, 24:295-300.
• [9]Ito M, Gilbert CD: Attention modulates contextual influences in the primary visual cortex of alert monkey. Neuron 1999, 22:593-604.
• [10]Motter BC: Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol 1993, 70:909-919.
• [11]McAdams CJ, Reid RC: Attention modulates the responses of simple cells in monkey primary visual cortex. J Neurosci 2005, 25:11023-11033.
• [12]McAlonan K, Cavanaugh J, Wurtz RH: Guarding the gateway to cortex with attention in visual thalamus. Nature 2008, 456:391-395.
• [13]Gandhi SP, Heeger DJ, Boynton GM: Spatial attention affects brain activity in human primary visual cortex. Proc Natl Acad Sci USA 1999, 96:3314-3319.
• [14]Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG: Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation. Neuron 1999, 22:751-761.
• [15]Silver MA, Ress D, Heeger DJ: Neural Correlates of Sustained Spatial Attention in Human Early Visual Cortex. J Neurophysiol 2007, 97:229-237.
• [16]Shulman GL, Corbetta MJA, Fiez JA, Buckner RL, Miezin FM, Raichle ME, Petersen SE: Searching for activations that generalize over tasks. Hum Brain Mapp 1997, 5:317-322.
• [17]Slotnick SD, Schwarzbach J, Yantis S: Attentional inhibition of visual processing in human striate and extrastriate cortex. Neuroimage 2003, 19:1602-1611.
• [18]Zani A, Proverbio AM: The timing of attentional modulation of visual processing as indexed by ERPs. In Neurobiology of attention. Edited by L Itti G, Rees JK, Tsotsos. San Diego (USA): Academic Press; 2005:514-519.
• [19]Fu S, Zinni M, Squire PN, Kumar R, Caggiano DM, Parasuraman R: When and where perceptual load interacts with voluntary visuospatial attention: An event-related potential and dipole modeling study. Neuroimage 2008, 39:1345-1355.
• [20]Fu S, Huang Y, Wang Y, Fedota J, Greenwood PM, Parasuraman R: Perceptual load interacts with involuntary attention at early processing stages: event-related potential studies. Neuroimage 2009, 48:191-199.
• [21]Fu S, Fedota JR, Greenwood PM, Parasuraman R: Dissociation of visual C1 and P1 components as a function of attentional load: An event-related potential study. Biol Psychol 2010, 85:171-178.
• [22]Kelly SP, Gomez-Ramirez M, Foxe JJ: Spatial Attention Modulates Initial Afferent Activity in Human Primary Visual Cortex. Cereb Cortex 2008, 18:2629-2636.
• [23]Rauss KS, Pourtois G, Vuilleumier P, Schwartz S: Attentional load modifies early activity in human primary visual cortex. Human Brain Mapping 2009, 30:1723-1733.
• [24]Zani A, Proverbio AM: ERP signs of early selective attention effects to check size. Electroencephalogr Clin Neurophysiol 1995, 95:277-92.
• [25]Zani A, Proverbio AM: Attention modulation of short latency ERPs by selective attention to conjunction of spatial frequency and location. J Psychophysiol 1997, 11:21-32.
• [26]Proverbio AM, Esposito P, Zani A: Early involvement of temporal area in attentional selection of grating orientation: an ERP study. Cogn Brain Res 2002, 13:139-151.
• [27]Khoe W, Mitchell JF, Reynolds JH, Hillyard SA: Exogenous attentional selection of transparent superimposed surfaces modulates early event related potentials. Vision Res 2005, 45:3004-3014.
• [28]Karns CM, Knight RT: Intermodal auditory, visual, and tactile attention modulates early stages of neural processing. J Cogn Neurosci 2008, 21:669-683.
• [29]Zani A, Proverbio AM: ERP signs of frontal and occipital processing of visual targets and distracters within and without the channel of spatial attention. In Focus on Neuropsychology Research. Edited by J Dupri. New York: Nova Science Publishers; 2006:38-88.
• [30]Zani A, Proverbio AM: Selective attention to spatial frequency gratings affects visual processing as early as 60 msec poststimulus. Percept Mot Skills 2009, 109:140-158.
• [31]Zani A, Proverbio AM: Attention modulation of C1 and P1 components of visual evoked potentials [abstract]. EEG Clin Neurophysiol 1997, 103:97.
• [32]Proverbio AM, Del Zotto M, Zani A: Electrical neuroimaging evidence that spatial frequency-based selective attention affects V1 activity as early as 40-60 ms in humans. BMC Neurosci 2010, 11:59. BioMed Central Full Text
• [33]Luck SJ, Hillyard SA, Mouloua M, Woldorff MG, Clark VP, Hawkins HL: Effects of spatial cuing on luminance detectability: Psychophysical and electrophysiological evidence for early selection. J Exp Psych: Hum Perc Perform 1994, 20:887-904.
• [34]Proverbio AM, Del Zotto M, Zani A: Inter-individual differences in the polarity of early visual responses and attention effects. Neurosci Let 2007, 419:131-136.
• [35]Stolarova M, Keil A, Moratti S: Modulation of the C1 Visual Event-related Component by Conditioned Stimuli: Evidence for Sensory Plasticity in Early Affective Perception. Cer Cortex 2006, 16:876-887.
• [36]Pourtois G, Grandjean D, Sander D, Vuilleumier P: Electrophysiological Correlates of Rapid Spatial Orienting Towards Fearful Faces. Cereb Cortex 2004, 14:619-633.
• [37]Proverbio AM, Riva F, Zani A, Martin E: Is it a baby? Perceived Age Affects Brain Processing of Faces Differently in Women and Men. J Cog Neurosci 2011, 23:3197-3208.
• [38]Proverbio AM, Adorni R, Zani A, Trestianu L: Sex differences in the brain response to affective scenes with or without humans. Neuropsychol 2009, 47:2374-2388.
• [39]Proverbio AM, Adorni R: C1 and P1 visual responses to words are enhanced by attention to orthographic vs lexical properties. Neurosci Let 2009, 463:228-233.
• [40]Rauss K, Schwartz S, Pourtois G: Top-down effects on early visual processing in humans: A predictive coding framework. Neurosci Biobehav Rev 2011, 35:1237.
• [41]Scerif G, Worden MS, Davidson M, Seiger L, Casey BJ: Context Modulates Early Stimulus Processing when Resolving Stimulus-Response Conflict. J Cog Neurosci 2006, 18:781-792.
• [42]Taylor MJ: Non-spatial attentional effects on P1. Clin Neurophysiol 2002, 113:1903-1908.
• [43]Thorpe S, Fize D, Marlot M: Speed of processing in the human visual processing. Nature 1996, 381:520-522.
• [44]Tanaka J, Luu P, Weisbrod M, Kiefer M: Tracking the time course of object categorization using event-related potentials. NeuroRep 1999, 10:829-835.
• [45]Proverbio AM, Del Zotto M, Zani A: The emergence of semantic categorization in early visual processing: ERP indices of animal vs artifact recognition. BMC Neurosci 2007, 8:24. doi: 10.1186/1471-2202-8-24 BioMed Central Full Text
• [46]Wijers AA, Mulder G, Okita T, Mulder LJM: An ERP study on memory search and selective attention to letter size and conjunctions of letter size and color. Psychophysiol 1989, 26:529-547.
• [47]Mangun GR, Hillyard SA, Luck SJ: Electrocortical substrates of visual selective attention. In Attention and Performance XIV. Edited by E Meyer, S Kornblum. Cambridge, MA: The MIT Press; 1993:219-243.
• [48]Schmidt T, Haberkamp A, Veltkamp GM, Weber A, Seydell-Greenwald A, Schmidt F: Visual processing in rapid chase systems: image processing, attention, and awareness. Front Psychol 2011, 2:doi: 10.33839/fpsyg.2011.00169.
• [49]Yamagishi N, Callan DE, Goda N, Anderson SJ, Yoshida Y, Kawato M: Attentional modulation of oscillatory activity in human visual cortex. Neuroimage 2003, 20:98-113.
• [50]Rihs TA, Michel CM, Thut G: A bias for posterior alpha-band power suppression versus enhancement during shifting versus maintenance of spatial attention. Neuroimage 2009, 44:190-199.
• [51]Romei V, Gross J, Thut G: On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J Neurosci 2010, 30:8692-8697.
• [52]Capotosto P, Babiloni C, Romani GL, Corbetta M: Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms. J Neurosci 2009, 6:5683-5683.
• [53]Banerjee S, Snyder AC, Molholm S, Foxe JJ: Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: Supramodal or sensory-specific control mechanisms? J Neurosci 2011, 31:9923-9932.
• [54]Roelfsema PR, Lamme VAF, Spekreijse H: Object-based attention in the primary visual cortex of the macaque monkey. Nature 1998, 395:376-381.
• [55]Vecera SP, Farah MJ: Does visual attention select objects or locations? J Exp Psychol: Gen 1994, 123:146-160.
• [56]Simon-Thomas ER, Brodsky K, Willing C, Sinha R, Knight RT: Distributed neural activity during object, spatial and integrated processing in humans. Cog Brain Res 2003, 16:457-467.
• [57]Foxe JJ, Simpson GV: Flow of activation from V1 to frontal cortex in humans: a framework for defining "early" visual processing. Exp Brain Res 2002, 142:139-150.
• [58]Wang J, Zhou T, Qiu M, Du A, Cai K, Wang Z, Zhou C, Meng M, Zhuo Y, Fan S, Chen L: Relationship between ventral stream for object vision and dorsal stream for spatial vision: An fMRI+ERP study. Hum Brain Map 1999, 8:170-181.
• [59]Olson CR, Gettner S: Brain representation of object-centered space. Curr Opin Neurobiol 1996, 6:165-170.
• [60]Motter BC: Neural correlates of attentive selection for color or luminance in extrastriate area V4. J Neurosci 1994, 14:2178-2189.
• [61]Treue S, Martinez Trujillo JC: Feature-based attention influences motion processing gain in macaque visual cortex. Nature 1999, 399:575-579.
• [62]Saenz M, Buracas GT, Boynton GM: Global effects of feature-based attention in human visual cortex. Nat Neurosci 2002, 5:631-632.
• [63]Hopf J-M, Boelmans K, Schenfeld MA, Luck S, Heinze H-J: Attention to features precedes attention to locations in visual search: Evidence from electromagnetic brain responses in humans. J Neurosci 2004, 24:1822-1832.
• [64]Woodman GF, Arita JT, Luck S: A cuing study of the N2pc component: An index of attentional deployment to objects rather than spatial locations. Brain Res 2009, 1297:101-111.
• [65]Clark VP, Hillyard SA: Spatial selective attention affects early extrastriate but not striate components of the visual evoked potentials. J Cogn Neurosci 1996, 8:387-402.
• [66]Zhang Y, Meyers EM, Bichot NP, Serre T, Poggio TA, Desimone R: Object decoding with attention in inferior temporal cortex. Proc Nat Acad Sciences 2011, 108:8850-8855.
• [67]Reuter-Lorentz PA, Kinsbourne M, Moscovitch M: Hemispheric control of spatial attention. Brain Cogn 1990, 12:240-266.
• [68]Robertson LC, Lamb MR, Knight RT: Effects of lesions of temporal-parietal junction on perceptual and attentional processing in humans. J Neurosci 1988, 10:3757-3789.
• [69]Palmer T, Tzeng OJ: Cerebral asymmetry in visual attention. Brain Cogn 1990, 13:46-58.
• [70]Mangun GR, Hinrichs H, Scholz M, Mueller-Gartner HW, Herzog H, Krause BJ, Tellman L, Kemma L, Heinze HJ: Integrating electrophysiology and neuroimaging of spatial selective attention to simple isolated visual stimuli. Vision Res 2001, 41:1423-1435.
• [71]Corbetta M, Miezin FM, Shulman GL, Petersen SE: A PET study of visuospatial attention. J Neurosci 1993, 13:1202-1226.
• [72]Corbetta M, Shulman GL, Miezin FM, Petersen SE: Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 1995, 270:802-805.
• [73]Fink GR, Halligan PW, Marshall JC, Frith CD, Frackowiak RS, Dolan RJ: Neural mechanisms involved in the processing of global and local aspects of hierarchically organized visual stimuli. Brain 1997, 120:1779-1791.
• [74]Fink GR, Dolan RJ, Halligan PW, Marshall JC, Frith CD: Space-based and object-based visual attention: shared and specific neural domains. Brain 1997, 120:2013-2028.
• [75]Federmeier KD, Kutas M: Picture the difference: electrophysiological investigations of picture processing in the two cerebral hemispheres. Neuropsychol 2002, 40:730-747.
• [76]Torralba A, Oliva A: Statistics of natural image categories. Network 2003, 14:391-412.
• [77]Tranel D, Damasio H, Damasio AR: A neural basis for the retrieval of conceptual knowledge. Neuropsychol 1997, 35:1319-1327.
• [78]Keil MS: Does face image statistics predict a preferred spatial frequency for human face processing? Proc Royal Soci B: Biol Sci 2008, 275:2095-2100.
• [79]Guyader N, Chauvin A, Peyrin C, Herault J, Marendaz C: Image phase or amplitude? Rapid scene categorization is an amplitude-based process. CR Biologies 2004, 327:313-318.
• [80]Kaping D, Tzvetanov T, Treue T: Adaptation to statistical properties of visual scenes biases rapid categorization. Vis Cogni 2007, 15:12-19.
• [81]Rossion B, Caharel S: ERP evidence for the speed of face categorization in the human brain: Disentangling the contribution of low-level visual cues from face perception. Vis Res 2011, 51(12):1297-1311.
• [82]Grill-Spector K, Kanwisher N: Visual recognition: as soon as you know it is there, you know what it is. Psychol Sci 2005, 16:152-160.
• [83]Roelfsema PR, Lamme VAF, Spekreijse H, Bosch H: Figure-ground segregation in a recurrent network architecture. J Cogn Neurosci 2002, 14:525-537.
• [84]Roelfsema PR: Cortical algorithms for perceptual grouping. Annu Rev Neurosci 2006, 29:203-227.
• [85]Hedgè J: Time course of visual perception: coarse-to-fine processing and beyond. Prog Neurobiol 2008, 84:405-439.
• [86]Kirchner H, Thorpe SJ: Ultra-rapid object detection with saccadic eye movements: visual processing speed revisited. Vision Res 2006, 46:1762-1776.
• [87]Mack ML, Palmeri TJ: The timing of visual object categorization. Front Psychol 2011, 2:doi: 10.33839/fpsyg.2011.00165.
• [88]de la Rosa S, Chouderry RN, Chatziastros A: Visual object detection, categorization, and identification tasks are associated with different time courses and sensitivities. J Exp Psychol Hum Percept Perform 2011, 37:38-47.
• [89]Mack ML, Gauthier I, Sadr J, Palmeri TJ: Object detection and basic level categorization: sometimes you know it is there before you know what it is. Psychon Bull Rev 2008, 15:28-35.
• [90]Shin K, Stolte M, Chong SC: The effect of spatial attention on invisible stimuli. Attn Percept Psychophys 2009, 71:1507-1513.
• [91]Schmidt F, Schmidt T: Feature-based attention to unconscious shapes and colors. Attn Percept Psychophys 2010, 72:112-118.
• [92]Lamme VAF: The difference between visual attention and awareness: a cognitive neuroscience perspective. In Neurobiology of Attention. Edited by L Itti G, Rees JK Tsotsos. San Diego: Elsevier Academic Press; 2005:167-174.
• [93]Koch C, Tsuchiya N: Attention and consciousness: two distinct brain processes. Trends Cogn Sci 2007, 11:16-22.
• [94]Li W, Piech V, Gilbert CD: Contour saliency in primary visual cortex. Neuron 2006, 50:951-962.
• [95]McManus JNJ, Li W, Gilbert CD: Adaptive shape processing in primary visual cortex. Proc Natl Acad Sci USA 2011, 108:9739-9746.