Neural mechanisms of visual backward masking revealed by high temporal resolution imaging of human brain

Backward masking is one of the potent ways to reveal the neural mechanism of visual awareness in humans. Although previous neuroimaging studies have reported that the visual masking involves the attenuation of hemodynamic signals to the masked stimulus in visual ventral regions such as the fusiform and inferior temporal gyrus, the temporal profiles of this attenuation as a whole neural population is mostly unclear. Here we used magnetoencephalography and investigated the neural response changes in higher visual region induced by backward masking. The combination of our previous random dot blinking method with the sensor-based analysis isolated the neural responses in the higher visual cortex relating to shape perception. The results revealed that, as the visibility of the target stimulus was reduced by the mask following it, the neural response to the target in the ventral regions showed gradual decreases both in its peak amplitude and peak latency. Furthermore, this decrease in the peak amplitudes was significantly correlated with the behavioral accuracy of the target identification, while the peak latency was not. These results indicate that backward masking simultaneously produces two types of neural changes in higher visual regions: attenuation of the populational neural activity itself and temporal interruption of this activity by the subsequent mask response. Especially, our data suggest that the response attenuation in higher visual response is a main cause of the perceptual impairment observed in the backward masking paradigm.

[1]  M Brázdil,et al.  Effect of subthreshold target stimuli on event-related potentials. , 1998, Electroencephalography and clinical neurophysiology.

[2]  J. Enns,et al.  What’s new in visual masking? , 2000, Trends in Cognitive Sciences.

[3]  M. Turvey On peripheral and central processes in vision: inferences from an information-processing analysis of masking with patterned stimuli. , 1973, Psychological review.

[4]  H. Spekreijse,et al.  Masking Interrupts Figure-Ground Signals in V1 , 2002, Journal of Cognitive Neuroscience.

[5]  T. Albright,et al.  Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1 , 1997, Visual Neuroscience.

[6]  R. Hari,et al.  Visual awareness of objects correlates with activity of right occipital cortex , 1996, Neuroreport.

[7]  R. Kakigi,et al.  Random dots blinking: a new approach to elucidate the activities of the extrastriate cortex in humans , 1998, Neuroreport.

[8]  Bruno G. Breitmeyer,et al.  Visual masking : an integrative approach , 1984 .

[9]  C. Summerfield,et al.  Induced gamma activity is associated with conscious awareness of pattern masked nouns. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[10]  Leanne M Williams,et al.  Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures , 2004, Human brain mapping.

[11]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[12]  Koji Inui,et al.  Temporal Dynamics of Neural Adaptation Effect in the Human Visual Ventral Stream , 2004, The Journal of Neuroscience.

[13]  Moshe Bar,et al.  Viewpoint Dependency in Visual Object Recognition Does Not Necessarily Imply Viewer-Centered Representation , 2001, Journal of Cognitive Neuroscience.

[14]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[15]  P. H. Schiller Single unit analysis of backward visual masking and metacontrast in the cat lateral geniculate nucleus. , 1968, Vision research.

[16]  S. Hillyard,et al.  Delayed Striate Cortical Activation during Spatial Attention , 2002, Neuron.

[17]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[18]  G. Orban,et al.  Processing of kinetically defined boundaries in areas V1 and V2 of the macaque monkey. , 2000, Journal of neurophysiology.

[19]  Eric Halgren,et al.  Cortical activation to illusory shapes as measured with magnetoencephalography , 2003, NeuroImage.

[20]  B G Breitmeyer,et al.  Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. , 1976, Psychological review.

[21]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[22]  E. Rolls,et al.  The Neurophysiology of Backward Visual Masking: Information Analysis , 1999, Journal of Cognitive Neuroscience.

[23]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

[24]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[25]  G Kovács,et al.  Cortical correlate of pattern backward masking. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

[27]  Hiroki Nakata,et al.  Gating of somatosensory evoked magnetic fields during the preparatory period of self-initiated finger movement , 2003, NeuroImage.

[28]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[29]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[30]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[31]  E. G. J. Eijkman,et al.  Cat optic tract and geniculate unit responses corresponding to human visual masking effects , 1972, Experimental Brain Research.

[32]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

[33]  Edmund T Rolls,et al.  Consciousness absent and present: a neurophysiological exploration. , 2004, Progress in brain research.

[34]  D. Kahneman Method, findings, and theory in studies of visual masking. , 1968, Psychological bulletin.

[35]  M. Livingstone,et al.  Neuronal correlates of visibility and invisibility in the primate visual system , 1998, Nature Neuroscience.

[36]  R Salmelin,et al.  Information processing in the human brain: magnetoencephalographic approach. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[38]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.