Abstract
Purpose.
The frequency-doubling (FD) phenomenon describes the increase in
apparent spatial frequency occurring when low-spatial-frequency sine
wave gratings undergo rapid counterphase flicker. It is unclear whether
the visual mechanisms isolated when pattern appearance is used as a
threshold criterion are the same as when a simple detection criterion
(as in FD perimetry) is used. It is also unclear whether the FD
stimulus isolates mechanisms that differ from those isolated by
spatially uniform flicker. In the current study, adaptation and
spatiotemporal tuning functions were determined, using the FD stimulus,
uniform flicker, and static (nonflickering) grating targets, to
establish whether distinct mechanisms are isolated by the FD stimulus.
methods. Spatiotemporal tuning functions were determined in six observers, using
an FD stimulus under conditions of detection and resolution and using
spatially uniform flickering stimuli and static grating stimuli. The
effect of light adaptation on these stimulus classes was also assessed.
All stimuli were 10°-wide squares.
results. Spatiotemporal tuning functions and adaptation characteristics were
identical for both the FD detection and resolution paradigms. Spatially
uniform flicker gave indistinguishable tuning functions and adaptation
characteristics to the FD stimulus at 25 Hz and higher, but differed
below this frequency. Static grating stimuli differed from FD stimuli
in both tuning functions and adaptation characteristics.
conclusions. Absolute detection of the FD stimulus involves mechanisms that are
indistinguishable from those involved when a criterion based on spatial
form (i.e., resolution of a pattern) is used, indicating that a simple
detection criterion can be used in FD perimetry. The FD stimulus
isolates similar mechanisms to spatially uniform flickering stimuli at
high temporal frequencies.
The frequency-doubling (FD) phenomenon was first described
by Kelly,
1 who observed that a low-spatial-frequency sine
wave grating appeared to double in spatial frequency when its contrast
was counterphase flickered at high rates. It has been shown that
contrast sensitivity to FD stimuli (i.e., low-spatial-frequency
gratings flickered at high temporal frequencies) is reduced in
glaucoma,
2 3 4 5 and FD stimuli have therefore been used in
the frequency-doubling technology (FDT) perimeter (Welch Allyn,
Skaneateles Falls, NY; and Humphrey Instruments, San Leandro, CA).
Maddess and Henry
6 have proposed that FD stimuli are
detected by M
y ganglion cells within the
magnocellular (M-cell) pathway. This and subsequent
5 work
used a method-of-adjustment psychophysical procedure to determine
thresholds, wherein subjects were instructed to use the appearance of
the FD pattern as a criterion. Suprathreshold targets have also been
used.
7 8 A criterion based on the appearance of the FD
pattern differs from that used in the FDT perimeter, in which subjects
typically respond to the perception of any stimulus, irrespective of
whether a frequency-doubled pattern is visible. Indeed, if the
perception of the FD pattern is used as a criterion in FDT perimetry,
abnormal results are frequently found in otherwise normal
subjects,
9 suggesting that the normative values used in
the perimeter are based on subjects responding to the perception of any
stimulus. It is unclear whether the appearance of a spatially doubled
pattern persists down to threshold for an FD stimulus, with some
investigators reporting that this occurs,
1 whereas others
suggest that a zone of amorphous flicker exists before the pattern
becomes visible
6 10 or that the grating stimulus returns
to close to its true spatial frequency.
11 As such, it is
possible that subjects responding to any percept in FDT perimetry are
obtaining flicker thresholds, which are also known to be reduced in
glaucoma.
12 13 14 15
Johnson and Demirel
14 used a uniform flickering patch of
the same size as the FD stimuli in the FDT perimeter, and found
sensitivities and specificities for the detection of glaucoma were only
slightly lower than when the FD stimulus was used. Such a result may be
interpreted in several ways. First, a large flickering stimulus and the
FD stimulus may both be detected preferentially by
M
y cells, as proposed by Maddess and
Henry.
6 Alternatively, the FD stimulus may only isolate a
discrete FD mechanism when a criterion based on spatial form is used
(e.g., as used by Maddess and Severt
5 and
Maddess and Henry
6 ), with simple detection
strategies (as used by Johnson and Demirel) isolating a different,
flicker-sensitive mechanism. As a third alternative, it is possible
that a number of spatiotemporally discrete stimuli (i.e., those
containing a limited range of spatial and temporal frequencies) can be
used to detect glaucomatous loss. In support of this latter
alternative, Johnson and Demirel
14 found that contrast
sensitivity to static (i.e., nonflickering), low-temporal-frequency
sine wave gratings gave only slightly lower glaucoma detection
sensitivities than both the FD and flickering stimulus. It is difficult
to assess whether the small differences in glaucoma sensitivity found
between FD, flickering, and nonflickering stimuli are significant,
owing to the relatively small number of subjects (
n =
16) investigated.
16
Therefore, it is not clear that simple detection strategies for the FD
stimulus isolate the same mechanism or mechanisms as when criteria
based on the perception of a spatial pattern are used. In addition, it
is not clear that the FD stimulus isolates a different mechanism or
mechanisms from a flickering, spatially uniform target. In this study,
we determined adaptation and spatiotemporal tuning functions using the
FD stimulus, a uniform flickering patch, and static grating targets, to
establish whether distinct mechanisms are isolated by the FD stimulus.
In addition, we examined what effect detection versus pattern
resolution criteria had on the mechanisms isolated by the FD stimulus.
Stimuli were presented on a calibrated video system [VSG 2/4
graphics card (Cambridge Research Systems Ltd., Kent, UK) and monitor
(CPD-G500, frame rate, 100 Hz; Sony, Tokyo, Japan)]. The monitor
subtended 62° × 48° (width × height) at the 33-cm viewing
distance. Ambient room illumination was dim.
Three stimulus classes were used: an FD stimulus (0.25–2 cyc/deg
gratings, counterphase flickered at 10–40 Hz), a uniform flickering
patch (0 cyc/deg, 10–40 Hz), and nonflickering (static) gratings
(0.25–2 cyc/deg). Stimulus contrasts were specified as Michelson
contrasts, presented in a raised cosine window of 1000 msec. The
minimum time between the offset of one stimulus and the onset of
another was 500 msec. All grating stimuli were oriented at 90°,
unless otherwise stated, and the spatial phase was random for each
presentation. All stimuli were 10°-wide squares, as used in the FDT
perimeter, and were presented centrally or at 15° eccentricity, as
measured from the center of the stimulus.
The FD stimulus was used in both a detection and an orientation
resolution paradigm. In the detection paradigm (FD detection), subjects
were permitted to respond to any attribute of the FD stimulus,
irrespective of whether spatial form was visible, hereinafter referred
to as a simple-detection criterion. In the orientation resolution
paradigm (FD resolution), subjects were forced to choose whether the
bars in the FD stimulus were oriented at 45° or 135°. Comparison of
the results from these two paradigms allows the effect that detection
versus pattern resolution criteria has on the mechanisms isolated by
the FD stimulus to be determined. For the principal author, detection
thresholds were measured using a two-interval, forced-choice paradigm,
and discrimination thresholds were measured using a two-alternative,
forced-choice paradigm. Forced-choice experiments were used to
eliminate any bias in this non-naïve observer. A ZEST
(zippy estimation by sequential testing) procedure
17 of 30
trials, which converged at the 88% correct level, was used to
manipulate contrast. In the remaining five observers, detection
thresholds were measured using a yes/no paradigm of eight trials, with
the ZEST procedure converging at the 78% correct level, and
discrimination thresholds were measured as for the principal author.
Thresholds from each subject were the geometric mean of at least two
measurements. Although the difference in convergence levels between the
forced-choice and yes/no paradigms would be expected to have a small
effect on absolute thresholds (0.05 log units, using a typical model of
the psychometric function
17 ), there is no effect on the
relative thresholds used in all the analyses presented in this article.
Paradigm (detection or discrimination) and background luminance were
kept constant during each experimental run, whereas spatial frequencies
were interleaved.
Six subjects, aged 29 to 51 years and with corrected vision
better than or equal to 20/20, participated in the experiments. All
subjects had no history of eye disease. Each subject viewed the monitor
monocularly with his or her preferred eye and natural pupils, and
fixation was maintained with a small, dark marker in the center of the
monitor. Three subjects had a history of migraine, but all were
required to have normal field results on the FDT perimeter. The study
complied with the tenets of the Declaration of Helsinki and was
approved by our institutional human experimentation committee, with all
subjects giving informed consent before participation.
Our results demonstrate that the mechanisms underlying sensitivity
to the FD stimulus can be differentiated from those underlying
spatially uniform flicker and static contrast sensitivity through the
use of adaptation and spatiotemporal tuning characteristics.
The spatiotemporal tuning functions measured with an FD stimulus had
identical shapes for both simple-detection and resolution criteria
(Figs. 3 4) . This unity was preserved under differing levels of light
adaptation, both when the entire field changed luminance
(Fig. 1) and
when only the stimulus area changed luminance
(Fig. 2) . These findings
demonstrate that simple-detection strategies isolate the same mechanism
or mechanisms as when criteria based on the appearance of spatial
structure (as used by Maddess et al.,
4 Maddess and
Henry,
6 and Bedford et al.
7 ) are used. As
such, subjects performing FDT perimetry should be instructed to respond
to the perception of any target, which appears to be the criterion on
which the normative database in the perimeter is based.
9 Although absolute sensitivity may vary, depending on the criterion used
in FDT perimetry,
9 32 the mechanisms isolated do not.
These findings also emphasize the importance of the instructions given
to patients undergoing FDT perimetric testing, a result that has also
been reported for standard automated perimetry.
33
We found no evidence that spatially uniform flicker differs from an FD
stimulus at 25 Hz and above, because both have indistinguishable
adaptation and temporal tuning characteristics. We confirm therefore
the hypothesis that FD stimuli and large, rapidly flickering targets
isolate similar underlying mechanisms.
6 Given this, it is
not surprising that spatially uniform flicker and an FD stimulus were
found to have similar specificities and sensitivities for the detection
of glaucoma.
14 The temporal-tuning characteristics of the
two stimuli differed below 25 Hz
(Fig. 3) , however, suggesting a
divergence in the mechanisms isolated at these lower temporal
frequencies. It is known that the visibility of the FD phenomenon
decreases as temporal frequency decreases,
7 10 34 35 and
so it is possible that the spatial frequency of the FD stimulus ceased
to appeared doubled at these lower temporal frequencies. This loss of
the FD phenomenon may relate to the observed divergence between flicker
and FD sensitivity, although this was not tested in our experiments.
Spatial-tuning characteristics
(Fig. 4) and adaptation characteristics
(Figs. 1 2) were significantly different between the FD stimulus and
static gratings, suggesting that the two stimuli isolate different
mechanisms within the visual system. Despite this difference, Johnson
and Demirel
14 found static gratings to have only slightly
lower specificities and sensitivities for the detection of glaucoma
than did the FD stimulus. These findings suggest that many
spatiotemporally discrete stimuli that are preferentially detected by a
single visual filter may successfully detect glaucomatous loss, because
redundant filters do not exist to mask any small losses of
sensitivity.
36 As such, the success of FDT perimetry in
detecting glaucoma
2 3 37 38 39 40 may not be that its stimuli
are detected by a pathway that is preferentially damaged by
glaucoma,
6 but more that its stimuli are more
spatiotemporally discrete than those used in conventional
increment-threshold perimetry.
In conclusion, we found that the mechanism or mechanisms isolated by
the FD stimulus were indistinguishable when subjects responded to any
percept (simple-detection) from when they respond to a distinct spatial
form (i.e., the appearance of a striped pattern). At a temporal
frequency of 25 Hz or greater, we found evidence that that the FD
stimulus isolated mechanisms similar to those isolated by a spatially
uniform flickering patch.
Supported by National Eye Institute Research Grant EY03424 (CAJ).
Submitted for publication July 13, 2001; revised September 21, 2001;
accepted October 18, 2001.
Commercial relationships policy: F, C (CAJ); N (AJA).
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked“
advertisement” in accordance with 18 U.S.C. §1734
solely to indicate this fact.
Corresponding author: Chris A. Johnson, Discoveries in Sight, Devers
Eye Institute, 1225 NE Second Avenue, Portland OR 97232;
[email protected].
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