Visuo-spatial neural response interactions in early cortical processing during a simple reaction time task: a high-density electrical mapping study

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Abstract

The timecourse and scalp topography of interactions between neural responses to stimuli in different visual quadrants, straddling either the vertical or horizontal meridian, were studied in 15 subjects. Visual evoked potentials (VEPs) were recorded from 64 electrodes during a simple reaction time (RT) task. VEPs to single stimuli displayed in different quadrants were summed (‘sum’) and compared to the VEP response from simultaneous stimulation of the same two quadrants (‘pair’). These responses would be equivalent if the neural responses to the single stimuli were independent. Divergence between the ‘pair’ and ‘sum’ VEPs indicates a neural response interaction. In each visual field, interactions occurred within 72–86 ms post-stimulus over parieto-occipital brain regions. Independent of visual quadrant, RTs were faster for stimulus pairs than single stimuli. This replicates the redundant target effect (RTE) observed for bilateral stimulus pairs and generalizes the RTE to unilateral stimulus pairs. Using Miller's ‘race’ model inequality (Miller J. Divided attention: evidence for coactivation with redundant signals, Cognitive Psychology 1982;14:247–79), we found that probability summation could fully account for the RTE in each visual field. Although measurements from voltage waveforms replicated the observation of earlier peak P1 latencies for the ‘pair’ versus ‘sum’ comparison (Miniussi C, Girelli M, Marzi CA. Neural site of the redundant target effect: electrophysiological evidence. Journal of Cognitive Neuroscience 1998;10:216–30), this did not hold with measurements taken from second derivative (scalp current density) waveforms. Since interaction effects for bilateral stimulus pairs occurred within 86 ms and require interhemispheric transfer, transcallosal volleys must arrive within 86 ms, which is earlier than previously calculated. Interaction effects for bilateral conditions were delayed by ≈10 ms versus unilateral conditions, consistent with current estimates of interhemispheric transmission time. Interaction effects place an upper limit on the time required for neuronal ensembles to combine inputs from different quadrants of visual space (≈72 ms for unilateral and ≈82 ms for bilateral conditions).

Introduction

Visual space is perceived as a unitary whole, although its initial cortical representation is divided between cerebral hemispheres and further divided between upper and lower banks of the calcarine sulcus. Normal visual perception, therefore, relies on recombination of these anatomically separated representations of visual space. This study used neurophysiological and behavioral methods to examine the mechanisms by which the brain combines inputs from different visual quadrants.

Interactions between responses to stimulus pairs appearing in different quadrants can be investigated by comparing summed visual evoked potentials (VEPs) to single stimuli presented in isolation to different quadrants with VEPs to the same stimuli, presented simultaneously as pairs. The summed VEP responses from single stimuli in two different quadrants (‘sum’) should be equivalent to the VEP from the same stimuli presented simultaneously (‘pair’) if neural responses to each of the single stimuli are independent. Divergence between ‘sum’ and ‘pair’ VEPs indicates an interaction between the neural responses to the spatially separated stimuli. Several forms of interaction effects have been reported from this comparison. For example, two studies have reported that the ‘sum’ and ‘pair’ VEPs superimpose until between 130 and 150 ms post-stimulus [1], [55]. Another study applied this comparison to reveal earlier peak P1 latencies for the ‘pair’ versus ‘sum’ condition [30], but did not report the latency of the interaction effect. However, visual inspection of these data (Fig. 9 of Ref. [30]) would suggest an effect substantially earlier than that reported by either Supek et al. [55] or Ahlfors et al. [1]. Moreover, while inter-hemispheric interactions have been examined through presentations of bilateral stimulus pairs, intra-hemispheric interactions between upper and lower quadrants, which would follow from presentation of unilateral stimulus pairs, have not been examined. The first goal of the present study was to determine the latency and scalp topography of neural response interactions between stimuli in different quadrants during a simple reaction time task.

A second focus of the current investigation was the reaction time facilitation seen when multiple stimuli are simultaneously presented (e.g. Refs. [18], [39]). During a visual simple reaction time (RT) task, wherein subjects make speeded responses to stimulus detection, RTs are faster when stimulus pairs are presented together than when single stimuli are presented in isolation. This RT facilitation has been termed the redundant target effect (RTE) and has been consistently observed in control subjects only under bilateral stimulation conditions [8], [27], [30], [41]. Whether this RTE also occurs in the case of unilateral stimulus pairs (upper and lower quadrants of the same hemifield) is unresolved. Two recent studies — one of patients with callosal pathology [20] and the other of hemispherectomized patients [57] — included a unilateral condition that resulted in an RTE facilitation. Problematic with generalizing this result to intact subjects is that neural reorganization in such patients has yet to be fully described (see Refs. [24], [66] for discussion). Moreover, two studies have found that the RTE following bilateral stimulus presentations could be accounted for by different models for patients and intact subjects [8], [41]. While the Tomaiuolo et al. study included an experiment with control subjects, there were very few trials per stimulus configuration and the stimuli in the bilateral and unilateral stimulus pair conditions were not at equal eccentricities [57]. To the best of our knowledge, the only other study of control subjects that included a unilateral condition at the same eccentricity as the bilateral condition did not show a consistent within-hemisphere RTE; with only one of the two subjects showing an RTE [41]. We first examined this issue of whether the RTE occurs for unilateral as well as bilateral stimulus pairs located at the same eccentricity from fixation.

A related issue concerns the necessity of neural interactions in producing the faster reaction times that define the RTE. Two classes of models of RT data have been proposed to explain the RTE: race models and coactivation models. In race models [39], neural interactions are not required to obtain the RTE. Rather, each stimulus of a pair independently competes for response initiation and the faster of the two mediates the response for any trial. Thus, simple probability summation could produce the RTE, since the likelihood of either of two stimuli yielding a fast reaction time is higher than that from one stimulus alone. In coactivation models [29], neural responses from stimulus pairs interact and are pooled prior to motor response initiation. The threshold for motor response initiation is met earlier for stimulus pairs than for single stimuli. We examined whether or not the race model could fully account for the RTE in each visual field. Violation of the race model would indicate that neural response interactions underlie this RT facilitation, in which case an electrophysiological correlate of the RTE might be expected.

An electrophysiological correlate of the RTE for bilateral stimulus pairs has been proposed [30]. Violation of the race model was associated with earlier peak P1 and N1 component latencies of the VEP recorded to stimulus pairs versus summed responses to single stimuli, apparently tracking the RTE [30]. While this comparison is appropriate for determining the latency of neural response interactions, it is inappropriate for determining if peak P1 latency tracks reaction time. Measurements based on summed data may yield a peak latency that is later than the faster of the two single stimulus responses, because the ‘sum’ VEP reflects contributions from both direct (contralateral) and indirect (ipsilateral) brain regions. This can be inferred from the absence of ipsilateral P1 and N1 components in patients with callosal agenesis as well as commisurotomy (reviewed in Ref. [5]). Likewise, previous research with neurologically normal subjects has shown that ipsilateral activity is prolonged by interhemispheric transfer time (IHTT; e.g. Ref. [47]). Peak P1 latency for the ‘sum’ condition will be measured at some time point between peak P1 latencies for the direct and indirect responses. The more stringent analysis is the comparison of the responses from the single stimuli with those from stimulus pairs, directly.

While this comparison was made in the Miniussi et al. [30] study, they describe that any amplitude or latency differences may have been the result of volume conduction and base their conclusions solely on the ‘pair’ versus ‘sum’ comparison. In order to minimize confounds of volume conduction, this analysis should be performed on the second spatial derivative of the scalp potential (also termed Laplacian or scalp current density). Indeed, recent research using this approach has revealed no support for a direct relationship between peak P1 latency and simple reaction times to single stimuli [46]. Using this Laplacian approach, we re-examined the relationship between peak P1 latency and reaction times in the context of bilateral and unilateral stimulus pairs. We reasoned that if peak P1 latency is directly related to the RTE, then peak P1 latency in the response to stimulus pairs should also be earlier than that in the response to each single stimulus as well as that from the summed single stimulus responses.

Section snippets

Subjects

Fifteen (seven female) neurologically normal, paid volunteers, aged 19–39 years (mean=26.5±5.4) participated. All subjects provided written informed consent and the Institutional Review Board of the Nathan Kline Research Institute approved the procedures. All subjects had normal or corrected-to-normal vision and were right-handed (Edinburgh Handedness Inventory; [35]).

Stimuli and procedure

Subjects were presented with ‘falsefont’ stimuli (Fig. 1a) that appeared white on a black background of a computer monitor

Neural interaction effects

The group-averaged SCD waveforms derived for 21 parieto-occipital scalp sites indicated that the response to stimulus pairs is of smaller amplitude than the summed responses from single stimuli. In order to determine when neural interactions between the responses to single stimuli reach statistical significance, we contrasted the response from the stimulus pair (‘pair’) and the summed responses from the single stimuli (‘sum’) by calculating point-wise paired t-tests (two-tailed) for each of the

Discussion

ERP responses to stimulus pairs presented simultaneously in different visual hemifields are not equivalent to the summed ERP responses to the constituent single stimuli presented in isolation. Assuming that stimuli have been appropriately lateralized, the difference between the summed and pair ERPs reflects neural response interactions following interhemispheric transfer. A similar rationale applies to stimulus pairs presented to upper and lower quadrants of the same visual hemifield. There are

Summary and conclusions

High-density VEP mapping revealed significant interactions between neural responses to stimuli presented simultaneously in separate visual quadrants during a simple reaction time task. These interactions began within ≈80 ms of stimulus onset and were observed both with unilateral stimulus pairs, straddling the horizontal meridian and with bilateral stimulus pairs, straddling the vertical meridian. Simple reaction times to stimulus pairs, distributed between quadrants either bilaterally or

Acknowledgements

The authors wish to thank Dr Clifford Saron for insightful discussions and Dr Martin Sliwinski for statistical expertise. Work supported by grants from the NIH (MH49334 and MH01439).

References (67)

  • R.C. Oldfield

    The assessment and analysis of handedness: The Edinburgh Inventory

    Neuropsychologia

    (1971)
  • F. Perrin et al.

    Spherical splines for scalp potential and current density mapping

    Electroencephalography and Clinical Neurophysiology

    (1989)
  • M.D. Rugg et al.

    Further investigation of evoked potentials elicited by lateralized stimuli: Effects of stimulus eccentricity and reference site

    Electroencephalography and Clinical Neurophysiology

    (1985)
  • M.D. Rugg et al.

    Visual evoked potentials to lateralized visual stimuli and the measurement of interhemispheric transfer time

    Neuropsychologia

    (1984)
  • M. Sugishita et al.

    Hemispheric representation of the central retina of commissurotomized subjects

    Neuropsychologia

    (1994)
  • S. Supek et al.

    Single vs. paired visual stimulation: superposition of early neuromagnetic responses and retinotopy in extrastriate cortex in humans

    Brain Research

    (1999)
  • C.M. Wessinger et al.

    Residual vision with awareness in the field contralateral to a partial or complete functional hemispherectomy

    Neuropsychologia

    (1996)
  • S.A. Ahlfors et al.

    Nonlinear spatial interactions in visual cortical responses revealed by high-density recordings of evoked potentials

    Society for Neuroscience Abstracts

    (1997)
  • G. Berlucchi et al.

    Influence of spatial stimulus–response compatibility on reaction time of ipsilateral and contralateral hand to lateralized light stimuli

    Journal of Experimental Psychology: Human Perception and Performance

    (1977)
  • G.S. Brindley

    The variability of human striate cortex

    Journal of Physiology (London)

    (1972)
  • V.P. Clark et al.

    Identification of early visual evoked potential generators by retinotopic and topographic analyses

    Human Brain Mapping

    (1995)
  • S. Clarke et al.

    Occipital cortex in man: organization of callosal connections, related myelo- and cytoarchitecture, and putative boundaries of functional visual areas

    Journal of Comparative Neurology

    (1990)
  • M.C. Corballis

    Interhemispheric neural summation in the absence of the corpus callosum

    Brain

    (1998)
  • E.A. DeYoe et al.

    Mapping striate and extrastriate visual areas in human cerebral cortex

    Proceedings of the National Academy of Sciences USA

    (1996)
  • D.J. Felleman et al.

    Distributed hierarchical processing in the primate cerebral cortex

    Cerebral Cortex

    (1991)
  • Foxe JJ, Simpson GV. Flow of activation from V1 to frontal cortex in humans: a framework for defining ‘early’ visual...
  • J.J. Foxe et al.

    Parieto-occipital ≈10 Hz activity reflects anticipatory state of visual attention mechanisms

    Neuroreport

    (2000)
  • M.H. Giard et al.

    Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study

    Journal of Cognitive Neuroscience

    (1999)
  • D. Guthrie et al.

    Significance testing of difference potentials

    Psychophysiology

    (1991)
  • M. Hershenson

    Reaction time as a measure of intersensory facilitation

    Journal of Experimental Psychology

    (1962)
  • M. Iacoboni et al.

    Parallel visuomotor processing in the split brain: cortico-subcortical interactions

    Brain

    (2000)
  • A. Ipata et al.

    Interhemispheric transfer of visual information in humans: the role of different callosal channels

    Archives of Italian Biology

    (1997)
  • M. Junghöfer et al.

    Mapping EEG-potentials on the surface of the brain: A strategy for uncovering cortical sources

    Brain Topography

    (1997)
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