Brain Research, Vol. 1368 (2011), p. 196 – 207
Time will tell: Deficits of temporal-information processing in patients with visual field loss Dorothe A. Poggela,b,*, Bernhard Treutweinc, Hans Strasburgera,b aGeneration
Research Program (GRP), Human Science Center, Ludwig-Maximilian University Munich, Prof.-Max-Lange-Platz 11, 83646 Bad Tölz, Germany bDepartment of Medical Psychology and Medical Sociology, University of Göttingen, Waldweg 37, 37073 Göttingen, Germany c IuK, Ludwig-Maximilian University Munich, Geschwister-Scholl-Platz 1, 80539 München, Germany
ARTICLE INFO
ABSTRACT
Article history: Accepted 17 Oct. 2010 Available online: 23 Oct. 2010
Visual field loss after brain lesions is commonly determined using perimetric tests of light detection (perimetry). Many patients with visual field defects complain about perceptual difficulties in areas that are perimetrically normal. To look at a potential cause for such difficulties, we topographically determined temporal characteristics of visual information processing in those patients and compared them to those of healthy subjects. In nine patients with visual field loss we measured thresholds of double-pulse resolution (DPR), i.e. the minimum perceivable duration of a temporal gap between two light pulses, at eccentricities up to 20°. Furthermore, high-resolution maps of visual reaction times (RT) were obtained in a computer based campimetric test. Performance was compared to healthy controls from a cross-sectional study of temporal perception across the life span. (Toelz Temporal Topography Study). Compared to healthy subjects, DPR thresholds and RTs in patients are elevated in the entire visual field, including areas that are perimetrically intact. Performance on temporal variables depends on the degree of intactness of the respective visual field position. DPR thresholds correlate considerably with RTs, and both parameters increase with eccentricity. However, whereas DPR thresholds are increased around blind regions relative to the intact field, this is not the case for RTs. Temporal processing in patients with cerebral vision loss is impaired to a certain extent independently from perimetric light-detection performance. This may partly explain reported subjective perceptual problems. The findings may have important implications for visual rehabilitation, i.e. the potential generalization of light detection training to temporal processing performance.
Keywords: temporal resolution, visual field defect, topography, reaction time, blindness, perimetry
* Corresponding Author. Department of Medical Psychology and Medical Sociology, University of Göttingen, Waldweg 37, 37073 Göttingen; Germany. Fax: +49-551-3913558 E-mail address:
[email protected] (D.A. Poggel). Abbreviations: DPR: double-pulse resolution; RT: reaction time, CFF: Critical flicker fusion:
BRAINRESEARCH1368(2011)196–207
1.
Introduction
Conventional perimetry of light detection is the method of choice for evaluating the intactness of the visual field (Harrington, 1981). However, many patients with visual field defects complain about difficulties of visual perception that cannot be identified with standard perimetry or other common clinical measures of visual function, e.g. in glaucoma (Horn et al., 1999; Tyler, 1981) but also after cortical damage (Castelo-Branco et al., 2006; Poggel, 2002). Hence, without additional testing, a patients’ complaints may appear groundless when in fact they may be a sign of undetected damage to the visual pathway or of beginning stages of a progressing disease. Topographical deviations between different visual functions may explain why some forms of visual impairment remain undetected in standard clinical testing (Bachmann and Fahle, 2000; Castelo-Branco et al., 2006). The variability of perimetric maps of different psychophysical measures in healthy individuals is not surprising given the high degree of functional specialization within the visual pathway, even at the earliest stages (e.g. between magno- and parvo-cellular systems (Callaway, 2005; DeYoe and Van Essen, 1988) and ventral vs. dorsal pathways beyond the primary visual cortex (Goodale et al., 2005; Mishkin and Ungerleider, 1982)). Hence, different test parameters may preferably reflect the function of different pathways in the visual system, resulting in different topographical distributions in the visual field (Silva et al., 2008). For instance, perimetric maps of luminance detection thresholds show little relation to the respective topographies of reaction times or letter contrast sensitivity (see Gothe et al., 2000; Poggel et al., 2004a; Poggel and Strasburger, 2004; Strasburger and Rentschler, 1996; Poggel et al., submitted). The situation becomes even more complex in patients with damage to the visual system because it is possible that lesions affect only parts of the visual pathway while others remain intact, thus again resulting in different topographic features of visual field maps (Bachmann and Fahle, 2000; Castelo-Branco et al., 2006). One dimension of visual perception that is mostly ignored in conventional clinical testing is temporal processing of visual information. An impairment of temporal-information processing may be caused by the same lesion that induces loss of other perceptual function, e.g. vision loss after damage to the primary visual cortex. Even without visual field defects, temporal processing may be impaired, however, resulting for instance in problems of temporal resolution or motion perception (Castelo-Branco et al., 2009b; Mendes et al., 2005). Such “secondary” defects would not normally be detected by conventional perimetry. The neural processing of time-related information and its relationship with sensory processes and their dynamic properties are still largely unknown or not well understood (Ivry and Spencer, 2004; Mauk and Buonomano, 2004; Poggel et al., 2004a; Poggel and Strasburger, 2004; Poggel et al., submitted). Processing temporal information proper, like estimating the duration of some event, seems a universal, supra-modal, and highly flexible capacity of the brain that is most likely supported by distributed cortical and subcortical networks (see Wittmann, 1999; Wittmann, 2009, for a review). Networks of temporal-information processing are probably closely connected to perceptual functions, similar to the close
197
interaction between perceptual and attentional functions. For example, some deficits of attention, e.g. spatial neglect, resemble perceptual deficits, and specific tests must be employed to differentiate attentional and perceptual impairments (Muller-Oehring et al., 2003). Temporal processing of visual information is performed at several levels, spanning from presumably low-level properties like those assessed by flicker fusion, to higher cognitive functions like the subjective estimation of temporal durations (see Wittmann, 1999). Here we are interested in two low-level process characteristics: temporal resolution and reaction times. The purpose of the present study is to examine whether and how these functions are affected by visual system lesions and whether their topographic distributions deviate from that of light detection performance. Some non-standard perimetric techniques are available for mapping temporal visual functions, including component perimetry (Bachmann and Fahle, 2000) and flicker perimetric methods (see McKendrick, 2005; Rota-Bartelink, 1999, for a review). Component perimetry simultaneously presents stimuli of a certain category across the visual field and tests the subjective perception of the defective area, particularly in patients with post-geniculate visual pathway lesions. While this method allows a fast test and an overview of potential defects, it does not include threshold testing or consider differences in temporal resolution across the visual field. To improve our understanding of the relationship between temporal processing and basic visual processes like light detection, it would be of interest to compare in more detail maps of conventional light detection thresholds with those of thresholds of temporal resolution. The various flicker perimetry approaches do allow for detailed mapping and also threshold testing. Their clinical application aims at uncovering retinal or other eye diseases, however, but they are not considered a standard part of ophthalmic examination in patients with post-geniculate defects. In addition, there are some methodological problems involved in the use of flicker stimulation (see below). Temporal resolution of visual stimuli has typically been measured by the critical flicker frequency (or flicker fusion, CFF), i.e. the threshold frequency at which a train of light pulses is perceived as non-flickering (Otto, 1987; Treutwein, 1989; Treutwein and Rentschler, 1992; Tyler, 1985; Tyler, 1987; Tyler and Hamer, 1990; Tyler and Hamer, 1993; Watson, 1986). Treutwein & Rentschler (1992) suggested using double pulses to measure temporal resolution by a transient stimulus – rather than by the steady-state response as in the CFF (see Rashbass, 1970) thus avoiding adaptation to flicker (Tyler, 1985; Tyler, 1987; Tyler and Hamer, 1990; Tyler and Hamer, 1993). Treutwein developed an adaptive maximum-likelihood method for measuring double pulse resolution (DPR) thresholds at multiple locations within one test (Treutwein, 1989; Treutwein and Rentschler, 1992). There are nine white square patches presented on a dark screen (one in the center, the other eight on a circle around it (see Methods). The presentation of the target patch is interrupted by a short temporal gap, i.e. it is a double pulse whereas the distracters are presented continuously. Treutwein excluded the influence of confounding cues like brightness differences from temporal summation or asynchrony in the test (Treutwein and Rentschler, 1992) so that the subject’s judgments reflect exclusively the minimal perceived temporal gap between light pulses at which the
198
BRAINRESEARCH1368(2011)196–207
stimuli can be perceived as two events (i.e. as flickering). As such, DPR performance might particularly reflect magnocellular pathway function and beyond the primary visual cortex area MT involvement both of which seem specialized in processing time-related information. Poggel et al. (Poggel et al., 2004a; Poggel and Strasburger, 2004; Poggel et al., 2006b) measured DPR thresholds across the visual field up to 20° eccentricity in a large sample of healthy subjects across the lifespan. DPR thresholds increased (i.e. sensitivity decreased) systematically and significantly with eccentricity, with a particularly steep rise within the central 5° radius. In part the increase of DPR thresholds stemmed from the fact that stimulus sizes were not scaled to compensate for the peripherally lower cortical magnification factor (Horton and Hoyt, 1991; see Drasdo, 1991 for a review}. To another part, however, the increase was explained by effects of sustained spatial attention through an increased size of the attentional focus and thus more diffuse attention (Poggel et al., 2006b). When these two factors were taken into account in a quantitative model, the temporal sensitivity in healthy subjects as measured by DPR thresholds was almost homogeneous within the inner 5° to 20° radius. DPR thresholds vary, however, over the life span, and the periphery of the visual field is affected by the aging process more than the visual field center (Poggel et al., 2004a; Poggel et al., submitted). Another important measure of low-level temporalinformation processing are simple reaction times (RTs) to light stimuli which have been examined in a wide range of studies on vision and visual attention (Becker et al., 2005; Luce, 1986; Schiefer et al., 2001; Teichner and Krebs, 1972; Wall et al., 2002). With respect to variation across the visual field the common finding is a small but rather systematic increase of RTs towards the periphery (on average 1.8 ms/deg; Schiefer, Strasburger, et al., 2001). This finding was confirmed in the Toelz Temporal Topography Study which showed a small but steady increase of RTs over the inner 20° radius (by 1.6 ms/ deg), i.e. much shallower than that for the DPR (Poggel et al., 2004a; Poggel et al., submitted). The mean (across the visual field) increase of RTs with increasing age in healthy adults is also steeper than the mean increase in DPR. At the same time, the increase of RTs happens in a more homogenous fashion, i.e. all visual field positions are affected in the same way in contrast to the stronger aging effect in the periphery for DPR (Bellis, 1933; Poggel et al., 2004a; Poggel et al., submitted). Earlier studies have shown that RTs are elevated in areas of residual vision at the border of blind areas in patients with partial visual field loss (Poggel, 2002; Poggel, Kasten, Mueller-Oehring, Bunzenthal, & Sabel, 2006; Poggel, Kasten, & Sabel, 2004). Hence, increased RTs may be an indicator of visual impairment even in areas outside a scotoma, similar to findings from non-conventional mapping studies described above (Bachmann and Fahle, 2000; Castelo-Branco et al., 2006; Castelo-Branco et al., 2009a). Differences in the topography and variation over the life span between DPR thresholds and RTs suggest that these two temporal parameters of visual information processing reflect partly separate mechanisms (Poggel et al., 2004b; Poggel et al., submitted). We were therefore interested whether DPR thresholds and RTs are elevated in patients with visual field loss. To put these results into perspective we
also determined the degree of similarity between the visual field distributions of RT and DPR and compared those topographies to perimetric maps. Deficits in the temporal characteristics of information processing might explain some of the perceptual difficulties in perimetrically intact visual field regions that are experienced by patients with visual field loss. For example, this phenomenon frequently occurs in glaucoma patients with respect to color perception and motion detection (Greenstein et al., 1996; Horn et al., 1999; Shabana et al., 2003; Tyler, 1981). Thus, the presence of functional loss before light detection deficits are detected in perimetry (like in glaucoma) or deficits in higher-order processing like temporal perception in areas clearly outside the perimetrically measured defects are of high diagnostic relevance. More generally, a dissociation between deficits of light perception and of temporal information processing on the behavioral level would contribute to the understanding of how closely those functions and their underlying neural structures are connected. Thus, in addition to the practical clinical value of the study, we expect insight on a basic visual neuroscience level regarding parallel distributed visual processing.
2.
Results
The grand mean DPR threshold (i.e. the minimal perceivable temporal gap between the double pulse targets) over all patients and test positions was 66.8 ms ± 6.6 ms SEM. DPR thresholds (averaged over the test positions of same eccentricity) increased significantly with eccentricity (Friedman Test χ2=19.8; df=3; p
