Hemispheric asymmetry in visual discrimination and memory: ERP evidence for the spatial frequency hypothesis

Event related potentials (ERPs) were recorded during delayed discrimination of simple spatial frequency gratings in the high and low frequency bands. Analyses of the waveforms N170, P220, N310, P400, and slow wave (SW) indicated significant and regionally specific interaction of spatial frequency and hemisphere for N170 amplitude. This interaction was independent of memory conditions, and appeared to be in the opposite direction of what is predicted by the spatial frequency model of hemispheric asymmetry. Additional interactions between spatial frequency and hemisphere were observed for N310 in the encoding process (reference stimulus) and for SW in the retrieval process (test stimulus). The general hypothesis of an interaction of spatial frequency and hemisphere in visual cognition is supported, but the findings indicate caution in interpreting an increase in physiological measures as an indication of more efficient brain processing. Moreover, several stages of information processing may contribute to the asymmetry observed in behavioral studies, and hemispheric balance may change dynamically during the time course of processing.

[1]  W Lang,et al.  Brain potentials with old/new distinction of non-words and geometric figures. , 1996, Electroencephalography and clinical neurophysiology.

[2]  J. Sergent The cerebral balance of power: confrontation or cooperation? , 1982, Journal of experimental psychology. Human perception and performance.

[3]  S Magnussen,et al.  The psychophysics of perceptual memory , 1999, Psychological research.

[4]  F. Kitterle,et al.  Hemispheric symmetry in contrast and orientation sensitivity , 1985, Perception & psychophysics.

[5]  Joseph B. Hellige,et al.  Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies , 1990, Perception & psychophysics.

[6]  Patrick Dupont,et al.  Human brain activity related to speed discrimination tasks , 1998, Experimental Brain Research.

[7]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[8]  Alice Mado Proverbio,et al.  Hemispheric Asymmetries for Spatial Frequency Discrimination in a Selective Attention Task , 1997, Brain and Cognition.

[9]  D. Schacter,et al.  Neuroimaging of Priming: New Perspectives on Implicit and Explicit Memory , 2001 .

[10]  S J Luck,et al.  Visual event-related potentials index focused attention within bilateral stimulus arrays. I. Evidence for early selection. , 1990, Electroencephalography and clinical neurophysiology.

[11]  Stephen Christman,et al.  Visual hemispheric asymmetries depend on which spatial frequencies are task relevant , 1992, Brain and Cognition.

[12]  E. DeYoe,et al.  Concurrent processing in the primate visual cortex. , 1995 .

[13]  David I. Perrett,et al.  Event-related potentials and the matching of familiar and unfamiliar faces , 1988, Neuropsychologia.

[14]  A. Proverbio,et al.  ERP signs of early selective attention effects to check size. , 1995, Electroencephalography and clinical neurophysiology.

[15]  M. Greenlee,et al.  Spatial-Frequency Discrimination, Brain Lateralisation, and Acute Intake of Alcohol , 1998, Perception.

[16]  D. Rose,et al.  An investigation into hemisphere differences in adaptation to contrast , 1983, Perception & psychophysics.

[17]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[18]  R Vogels,et al.  Human Brain Activity Related to Orientation Discrimination Tasks , 1997, The European journal of neuroscience.

[19]  T. Mergner,et al.  Delayed pattern discrimination in patients with unilateral temporal lobe damage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A Fiorentini,et al.  Right-Hemisphere Superiority in the Discrimination of Spatial Phase , 1984, Perception.

[21]  G. Mangun,et al.  Neural Mechanisms of Global and Local Processing: A Combined PET and ERP Study , 1998, Journal of Cognitive Neuroscience.

[22]  G. Orban,et al.  Regions in the human brain activated by simultaneous orientation discrimination: a study with positron emission tomography , 1998, The European journal of neuroscience.

[23]  Visual Field Differences in Spatial Frequency Discrimination , 1999, Brain and Cognition.

[24]  A Kok,et al.  Event-related potentials to conjunctions of spatial frequency and orientation as a function of stimulus parameters and response requirements. , 1993, Electroencephalography and clinical neurophysiology.

[25]  S. Magnussen Low-level memory processes in vision , 2000, Trends in Neurosciences.

[26]  A. Nowicka,et al.  VISUAL-SPATIAL-FREQUENCY MODEL OF CEREBRAL ASYMMETRY : A CRITICAL SURVEY OF BEHAVIORAL AND ELECTROPHYSIOLOGICAL STUDIES , 1996 .

[27]  G. Plant,et al.  Transient visually evoked potentials to the pattern reversal and onset of sinusoidal gratings. , 1983, Electroencephalography and clinical neurophysiology.

[28]  Peter Lennie,et al.  6 – PARALLEL PROCESSING OF VISUAL INFORMATION , 1989 .

[29]  S. Christman Chapter 1 - Hemispheric Asymmetry in the Processing of Spatial Frequency: Experiments Using Gratings and Bandpass Filtering. , 1997 .

[30]  H. Begleiter,et al.  A neurophysiologic correlate of visual short-term memory in humans. , 1993, Electroencephalography and clinical neurophysiology.

[31]  D. Spinelli,et al.  Contrast and hemispheric asymmetry: an electrophysiological investigation. , 1990, The International journal of neuroscience.

[32]  J P Thomas,et al.  Parallel processing in visual short-term memory. , 1996, Journal of experimental psychology. Human perception and performance.

[33]  A. Nowicka,et al.  Visual-spatial-frequency model of cerebral asymmetry: a critical survey of behavioral and electrophysiological studies. , 1996, Psychological bulletin.

[34]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[35]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[36]  F. Kitterle,et al.  Visual field effects in the discrimination of sine-wave gratings , 1991, Perception & psychophysics.

[37]  G A Orban,et al.  Human brain regions involved in direction discrimination. , 1998, Journal of neurophysiology.

[38]  John J. Foxe,et al.  Activation Timecourse of Ventral Visual Stream Object-recognition Areas: High Density Electrical Mapping of Perceptual Closure Processes , 2000, Journal of Cognitive Neuroscience.

[39]  D. Spinelli,et al.  Hemispheric asymmetry of pattern reversal visual evoked potentials in healthy subjects. , 1987, International Journal of Psychophysiology.

[40]  Luciano Mecacci,et al.  Chapter 2 – Temporal Frequency Processing , 1997 .

[41]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[42]  Francois Jouen,et al.  Spatial Frequency and Right Hemisphere: An Electrophysiological Investigation , 1998, Brain and Cognition.

[43]  Neocortical Areas underlying Visual Short-term Memory: Evidence from fMRI , 1998, NeuroImage.

[44]  V. Goffaux,et al.  Spatio-temporal localization of the face inversion effect: an event-related potentials study , 1999, Biological Psychology.

[45]  M. Viggiano,et al.  Hemispheric Asymmetry in Transient Visual Evoked Potentials Induced by the Spatial Factor of the Stimulation , 1993, Brain and Cognition.