Elsevier

Brain and Cognition

Volume 62, Issue 3, December 2006, Pages 214-220
Brain and Cognition

Effect of temporal constraints on hemispheric asymmetries during spatial frequency processing

https://doi.org/10.1016/j.bandc.2006.05.005Get rights and content

Abstract

Studies on functional hemispheric asymmetries have suggested that the right vs. left hemisphere should be predominantly involved in low vs. high spatial frequency (SF) analysis, respectively. By manipulating exposure duration of filtered natural scene images, we examined whether the temporal characteristics of SF analysis (i.e., the temporal precedence of low on high spatial frequencies) may interfere with hemispheric specialization. Results showed the classical hemispheric specialization pattern for brief exposure duration and a trend to a right hemisphere advantage irrespective of the SF content for longer exposure duration. The present study suggests that the hemispheric specialization pattern for visual information processing should be considered as a dynamic system, wherein the superiority of one hemisphere over the other could change according to the level of temporal constraints: the higher the temporal constraints of the task, the more the hemispheres are specialized in SF processing.

Introduction

Visual scenes are made up of several objects (e.g., houses, trees) themselves made up of smaller objects (e.g., windows, leaves). Convergent data from the functional neuro-anatomy of magnocellular and parvocellular visual pathways (Van Essen & DeYoe, 1995), neurophysiological recordings in primates (Bullier, 2001), and psychophysical results in humans (Ginsburg, 1986, Hughes et al., 1996) suggest that visual analysis of this hierarchical information is critically dependent on spatial frequency (SF) processing of the image with a preferential coarse-to-fine (CtF) processing sequence. The low spatial frequencies (LSF), conveyed by fast magnocellular visual pathways, might activate the visual areas first allowing an initial perceptual parsing of a visual scene. This initial low-pass visual analysis might then be refined by high spatial frequencies (HSF), conveyed more slowly by parvocellular visual pathways.

Experimental evidence in support of a CtF processing hierarchy in human vision comes from psychophysical studies using gratings of different SF as stimuli. For example, Breitmeyer, 1975, Breitmeyer and Ganz, 1977 showed that LSF channels have short latencies and short integration time, whereas HSF channels respond slowly and have a long integration time, suggesting thus that LSF are transmitted faster than HSF through the visual system. Additional evidence was provided by psychophysical studies using hierarchical forms, which are global forms composed of several local elements (see Navon, 1977). Classically, the global information is identified faster than the local elements. Based on the assumption that global information is preferentially conveyed by LSF whereas local information by HSF (Badcock et al., 1990, Hughes et al., 1996, Lamb and Yund, 1993), this global precedence effect has been interpreted as reflecting a fundamental principle of CtF analysis. Importantly, CtF analysis of SF was also demonstrated during the perception of more ecological visual stimuli, such as natural scene images. For example, Schyns and Oliva (1994) used a matching task with “hybrid” stimuli made of two superimposed images from natural scenes, belonging to different semantic categories and containing different SF-bands (e.g., a highway scene in LSF superimposed on a city scene in HSF). They showed that very brief presentation time of hybrids (30 ms) elicited matchings based on their LSF content while longer presentation time (150 ms) elicited matchings based on their HSF content. These results thus suggest a precedence of LSF on HSF over the course of scene recognition.

Within the framework of visual SF analysis, it has often been proposed that the right hemisphere (RH) might be predominantly involved in LSF information processing whereas the left hemisphere (LH) might be more involved in HSF processing. This assumption has been supported by numerous behavioural studies (Blanca et al., 1994, Chokron et al., 2000, Martin, 1979, Sergent, 1982) and neuroimaging studies (Fink et al., 1996, Han et al., 2002, Heinze et al., 1998, Lux et al., 2004, Martinez et al., 1997, Proverbio et al., 1998, Yamaguchi et al., 2000) conducted among healthy subjects, as well as neuropsychological observations (Lamb et al., 1990, Robertson and Lamb, 1991, Robertson et al., 1988) using hierarchical forms as stimuli. Typically, these studies observed a functional hemispheric specialization for global vs. local processing (i.e., a RH dominance for processing global information and a LH dominance for local information) that has been interpreted as reflecting a basic hemispheric specialization for low vs. high spatial frequency processing (see Grabowska and Nowicka, 1996, Ivry and Robertson, 1998, Sergent, 1982).

More direct evidence of hemispheric specialization in SF processing was provided by behavioural studies using gratings of different SF (Christman et al., 1991, Kitterle et al., 1990, Kitterle et al., 1992, Kitterle and Selig, 1991) or LSF and HSF natural pictures. Indeed, in recent divided visual field studies conducted on healthy participants, we addressed the issue of hemispheric specialization for SF processing by altering the frequency spectrum of natural scenes images (Peyrin et al., 2003, Peyrin et al., 2006). Our results showed that the two hemispheres differ significantly in the way they process SF. Results showed a left visual field/right hemisphere (LVF/RH) superiority during the recognition of LSF scene images, whereas a right visual field/left hemisphere (RVF/LH) superiority was observed during the recognition of HSF scene images, thus supporting the hypothesis of hemispheric specialization in the processing of SF (Sergent, 1982). Recent functional brain imaging studies conducted on healthy subjects also support this pattern of functional cerebral organization (Iidaka et al., 2004, Kenemans et al., 2000, Peyrin et al., 2004, Peyrin et al., 2005).

The aim of the present study was to specify the pattern of hemispheric specialization for SF with respect to the CtF hypothesis among healthy participants. For this purpose, we aimed to investigate the influence of stimuli presentation time on the LVF/RH and RVF/LH advantage for respectively LSF and HSF natural scene images. A few studies dealing with hierarchical form processing have investigated the influence of exposure duration on hemispheric specialization. For example, in a divided attention task, Blanca et al. (1994) found a classical global/local hemispheric specialization for short (50 ms), but not for longer (100 and 200 ms) exposure duration of hierarchical forms. The authors concluded that hemispheric specialization during global and local information processing only appears when the stimulus visibility is limited. Differently, in a selective attention task, Boles and Karner (1996) found an unexpected RH dominance for local processing that was stronger for short (33 ms) than long duration (100 ms). The authors concluded that hemispheric asymmetries found for short exposure duration might reflect a basic RH predominance in the processing of degraded visual stimuli, irrespective of their SF content. More recently, Evert and Kmen (2003) using a larger sample of exposure duration in a selective attention task found more consistently a LH dominance for local processing than a RH dominance for global processing. Furthermore, this LH specialization was most commonly observed in the middle range of exposure durations tested (e.g., 53 and 67 ms). Thus, these studies led to conflicting hypotheses about the effect of exposure duration on hemispheric specialization for global and local processing. Furthermore, none of these experiments were designed with regard to the CtF analysis of natural scenes.

Therefore, in pilot work, we used the divided visual field task of LSF and HSF natural scene recognition (see Peyrin et al., 2003, Peyrin et al., 2006), in which we simply manipulated exposure duration of scene stimuli. Exposure durations were chosen on the basis of Schyns and Oliva’s study (1994). Thus, scenes were displayed either for 30 ms (short presentation condition) or 150 ms (long presentation condition). However, results of this pilot work showed that filtered scenes briefly flashed for 30 ms in one visual hemifield were almost imperceptible for participants, suggesting that the task used was not appropriate to our investigations. Therefore, in the present study, we manipulated exposure duration independently of both SF content and visual field of presentation. For this purpose, we used matching task between two successive scene images. Based on Schyns and Oliva’s works (1994), (Experiment 1), exposure duration (either 30 or 150 ms) was manipulated on the first scene and always displayed in the central visual field (i.e., projected on both hemispheres). Based on our previous studies, the second scene was both filtered either in LSH or HSF and lateralized either in the LVF/RH or RVF/LH. Participants had to decide whether the two successive scenes were from the same category.

Our predictions were as follows: Under the hypothesis of hemispheric specialization for SF processing, we should observe a LVF/RH advantage when matching the second LSF scene and a RVF/LH advantage when matching HSF information. In addition, regarding the literature about CtF analysis of SF, variations in the presentation time of the first scene should change the SF band preferentially processed in the first non-filtered scene. Therefore, based on Schyns and Oliva’s study (1994), for short presentation time (30 ms), we expected participants to use LSF information in the first non-filtered scene. This ‘coarse’ analysis may preferentially recruit the RH (specialized for LSF processing) and thus predominantly engage this hemisphere for the subsequent matching process with the second scene. Conversely, for longer presentation (150 ms), we expected them to use HSF information. This more ‘fine’ analysis may preferentially engage the LH (specialized for HSF processing) in the processing of the whole scene sequence. Therefore, our main prediction was that brief relative to long presentations should enhance the LVF/RH advantage when matching the second LSF scene, whereas long presentation should enhance the LH advantage when matching the second HSF scene. On the contrary, if temporal constraints applied on the processing of the first scene have no effect on the matching process, we should expect similar patterns of hemispheric asymmetries irrespective of the first scene exposure duration (30 vs.150 ms).

Section snippets

Participants

Sixteen healthy undergraduate students of the Psychology from the Université Pierre Mendès-France in Grenoble (eight men and eight women) participated in the experiment for course credits. All were right-handed as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). All participants had normal or corrected-to-normal vision and they were not aware of the purpose of the experiment.

Stimuli

Stimuli were four black-and-white photographs (256 × 256 pixels, 256 grey-scales) of natural scene images:

Results

Mean correct reaction times in milliseconds (mRT), standard deviations (SD), and mean error rate (mER) for each experimental condition (Exposure duration × SF content × Visual field of presentation) are reported in Table 1. To reduce the effect of extreme values in calculating mRT, RT for each subject’s correct response in each condition was trimmed by removing responses inferior and superior to two standard deviations from the mean of each condition. This led to the exclusion of 4.49% of correct

Discussion

The aim of the present study was to investigate whether the temporal properties of SF processing might influence hemispheric specialization. With regard to the CtF analysis of SF, we predicted that the RH dominance in LSF information processing might be enhanced by a brief presentation of visual information while a longer presentation might enhance the LH dominance for processing HSF.

However, contrary to our predictions, results showed a classic hemispheric specialization pattern for SF

Acknowledgments

The authors wish to thank Cecilie Rondan and David Alleysson for their assistance. This research was funded by a fellowship from the Fondation Fyssen awarded to CP and MM, and by the National Centre for Scientific Research (CNRS UMR 5105) in France.

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