Vision Research 43 (2003) 617–627
www.elsevier.com/locate/visres
Senescence of the temporal impulse response to a luminous pulse
Keizo Shinomori
a,*
, John S. Werner
b
a
Department of Information Systems Engineering, Kochi University of Technology, 185 Miyanokuchi, Tosayamada-town,
Kami-gun, Kochi 782-8502, Japan
b
Department of Ophthalmology and Section of Neurobiology, Physiology and Behavior, University of California, Davis,
4860 Y Street, Suite 2400, Sacramento, CA 95817, USA
Received 9 September 2002; received in revised form 3 January 2003
Abstract
An impulse response function (IRF) to a luminous pulse was derived for 70 normal observers ranging in age from 16 to 86 years.
Thresholds were measured for two pulses separated by interstimulus intervals from 6.7 to 180 ms. The pulses had a spatial Gaussian
shape (1 SD ¼ 2:3° diam) and were presented as increments on a 10 cd/m2 background, having the same chromaticity as the pulse.
A spatial 4-alternative forced-choice method was combined with a staircase procedure. Retinal illuminance was equated individually
by heterochromatic flicker photometry and control of pupil area. Each IRF was measured four times, in separate sessions, for each
observer. IRFs calculated from the threshold data revealed significant age-related changes in the response amplitude of both excitatory and inhibitory phases. In general, there were no significant changes in the time to the first peak or in the first zero crossing.
For 12 of 20 observers over 60 years of age, however, the amplitude of the second (inhibitory) phase was reduced relative to the
excitatory phase so their IRFs were quite slow and long. Control conditions with three pseudophakic observers and two normal
observers with induced blur demonstrated that age-related changes in the IRF under these conditions cannot be ascribed to optical
factors. The data suggest that the human visual system generally maintains a stable speed of response to a flash until at least about
80 years of age, even while there are senescent reductions in response signal amplitude.
Ó 2003 Elsevier Science Ltd. All rights reserved.
1. Introduction
Senescent losses in temporal sensitivity of the human
visual system have been demonstrated extensively
through early studies of critical flicker frequency, the
lowest frequency of temporal modulation that is indiscriminable from a steady light (Coppinger, 1955; see
reviews by Kline & Scheiber, 1982; Weale, 1982). Part of
this loss in temporal vision is due to retinal illuminance
differences between younger and older observers. For
example, Wright and Drasdo (1985) (see also Kuyk &
Wesson, 1991) reported losses in contrast sensitivity to
sinusoidal flicker (3.3–30 Hz) that were greatest at
higher frequencies and they ascribed most of this change
to age-related decreases in pupillary area. This interpretation is supported by a shift in the temporal contrast
sensitivity function (tCSF) downward (lower sensitivity)
and to the left (lower temporal resolution, longer time
*
Corresponding author. Tel.: +81-8875-7-1020; fax: +81-8875-72220.
E-mail address: shinomori.keizo@kochi-tech.ac.jp (K. Shinomori).
constants) with reduced retinal illuminance (DeLange,
1958; Kelly, 1961) or equivalently, reductions in pupillary area (Mayer, Kim, Svingos, & Glucs, 1988).
Age-related reductions in retinal illuminance due to
increases in ocular media density could also contribute
to senescent losses in temporal contrast sensitivity, especially for stimuli that include short- and middle-wave
light (Werner, 1982; Weale, 1988). The effects of ocular
media senescence can be minimized by long-wave stimuli. Thus, Tyler (1989) used an LED with dominant
wavelength of 660 nm and found an age-related loss
after 16 years at high (20–30 Hz) but not low (5 Hz)
temporal frequencies. He interpreted these results in the
time domain as due to an impulse response with a
change in timing parameters (time to peak and duration
of excitatory response or zero crossing), but not amplitude. With the same apparatus, but incorporating a
forced-choice psychophysical procedure, Kim and
Mayer (1994) measured the tCSF of 89 observers (18–
77 years). They found changes after 44 years for
intermediate through high temporal frequencies (>7–
50 Hz). Calculated impulse response functions showed
0042-6989/03/$ - see front matter Ó 2003 Elsevier Science Ltd. All rights reserved.
doi:10.1016/S0042-6989(03)00009-9
618
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
significant age-related reductions in response amplitude
but not in time to the peak or in the zero crossing. There
is thus an inconsistency between these studies in the
nature of age-related changes in the IRF for luminance
modulation. It may be added that the latter two studies
used a relatively high luminance, long-wavelength test
stimulus which may have produced frequency-dependent adaptation at a post-receptoral site (Swanson,
1993). A subsequent study with a test stimulus of lower
retinal illuminance reported tCSFs consistent with those
of Mayer and Kim (Swanson, Fiedelman, & Fish, 1995).
The tCSF is commonly used for inferring the IRF,
however, it only provides information about amplitude
and does not preserve phase (Victor, 1989). A complementary basis for obtaining the IRF is to measure
thresholds for two consecutive pulses as a function of
the time between them, or inter-stimulus interval (ISI).
The shape of the IRF can be derived more accurately
using this double-pulse method because an auto-correlation function of the IRF can be obtained (Ikeda, 1965;
Rashbass, 1970; Watson & Nachmias, 1977; Uchikawa
& Yoshizawa, 1993) whereas measurement of tCSFs
provides only the maximum contrast in the convolution
between the impulse response and flicker threshold. The
two-pulse method was used to measure senescent
changes in the IRF in this study. We used the model of
Burr and Morrone (1993) to calculate the IRF from the
two-pulse detection data from a large group of observers, covering a broad age range, with controls for variation in retinal illuminance and psychophysical criterion.
We found significant age-related changes in IRF amplitude and a complex relation between aging and temporal parameters, with no change for most observers,
but an increase for some older observers due to the loss
of inhibitory phase.
2. Methods
2.1. Subjects
Seventy phakic (natural lenses) observers (32 males
and 38 females) ranging in age from 16 to 86 years
participated in this experiment. They were approximately evenly distributed across age (10 each decade)
and ethnically diverse. In addition, three pseudophakes
(subjects with an intraocular lens implant following
removal of a cataractous lens), 67–76 years, served as
controls for effects of retinal illuminance.
None of the subjects reported systemic, ocular or
neurological conditions known to disrupt vision. All
subjects received a complete optometric/ophthalmologic
examination in the Department of Ophthalmology at
the UC-Davis Medical Center. The presence of retinal
disease and abnormal ocular media in the tested eye
were ruled out by ocular examination including visual
acuity, slit lamp examination, and direct and indirect
ophthalmoscopy. Color stereo fundus photographs of
the macula and optic disc (ETDRS Fields 1 and 2) were
evaluated by a retinal specialist using a stereo viewer.
The retinae of all subjects were found to have no more
than five small ( 663 lm) drusen and no vascular, retinal, choroidal or optic nerve findings known to disrupt
visual function. Intraocular pressure was 622 mm Hg.
All subjects demonstrated a corrected Snellen acuity of
P20/30 in the tested eye, as well as normal color vision
when tested with the Neitz anomaloscope, the HRR
pseudoisochromatic plates and the Farnsworth F-2
plate. Subjects with refractive errors greater than +4.00
or )6.50 D were excluded.
Written informed consent was obtained following the
Tenets of Helsinki, and with approval of the Office of
Human Research Protection of the University of California, Davis, School of Medicine.
2.2. Apparatus and stimuli
Thresholds for contrast detection were measured by
presenting test stimuli as luminance increments on a 10
cd/m2 (1:69 log Td.) background of the same chromaticity (CIE x; y ¼ 0:33; 0:33). Two pulses (1.2 ms each
with interstimulus intervals ranging from 6.7 to 180 ms)
were presented in one of four quadrants defined by a
central fixation cross. The four positions of the test
stimuli were located 1.70° to one side or the other and
1.70° above or below the center of the fixation cross. A
Gaussian patch with a 2.26° diameter at 1 SD was chosen
for a test spatial profile to eliminate artifacts caused by
spatial transients. These stimuli were presented on a
CRT display (Sony GDM-200 PS) operating at a 150 Hz
frame rate that was controlled by a video board with 15bit resolution (Cambridge Research Systems, VSG 2/4)
using a Dell Pentium computer. A second CRT monitor
displayed the stimuli for the experimenter.
An astronomical telescope was focused so that the
subject viewed the CRT at optical infinity with a 2.16
magnification. A 5.0 mm aperture stop was positioned
in front of the telescope objective such that the 2.5 mm
image of the stop formed the exit pupil of the optical
system in the plane of the subjectÕs anatomical pupil.
Trial lenses were mounted in a holder positioned in front
of the eye to correct individual refractive error. An adjustable chair and a dental-impression bite-bar assembly, with movement in three orthogonal directions, were
used to maintain the subjectÕs position. A pellicle was
placed in the optical path so that light from the subjectÕs
eye was directed into an auxiliary optical system. Using
a reticule aligned with the optic axis of the telescope, this
auxiliary system permitted precise alignment of the
subjectÕs pupil. The display monitor, optical system and
subject were enclosed within a light-tight viewing lane.
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
2.3. Calibrations
A spectroradiometer/photometer (Photo Research,
Model PR703-A) and a chromameter (Minolta, CS-100)
were used to measure the luminance and chromaticity
coordinates of the CRT phosphors. A gamma correction
to linearize the relation between phosphor radiance and
voltage was based on lookup tables using a photodiode
and calibration software in the VSG software (Cambridge Research Systems, OptiCal).
Rise and fall times of the CRT phosphors were
measured with a p–i–n 10 silicon photodiode (United
Detector technology, Optometer 81, 10 mm diameter)
connected to a digital oscilloscope. Intensity increments
and decrements were 1.2 ms for all phosphors. Because
the diameter of the Gaussian patch at 1 SD was 106
pixels on a 640 480 pixel display, the decay of the test
stimulus at the vertical scan frequency was less than 1.5
ms from the maximum. Peak-to-peak timing error of
the ISI was <3%.
619
by lenticular senescence, and because the optical system
produced an image of the stimulus in the plane of the
pupil that was smaller (2.5 mm diameter) than that expected for observers spanning our age range (Loewenfeld, 1979), it follows that retinal illuminance was
equated across observers.
Following 5 min dark adaptation and 10 min adaptation to the background, subjects were presented with
test stimuli preceded by a high pitch tone and followed
by a low pitch tone. The subjectÕs task was to press one
of four buttons to indicate the quadrant in which the
stimulus was detected. This 4-alternative forced-choice
(4AFC) method was combined with a two-down, one-up
staircase in which the luminance of both pulses was
changed simultaneously to obtain a contrast threshold.
Thresholds were based on the last four of six reversals,
corresponding to a probability of 70.7% detection. During each session the 14 ISI settings were tested with 14
different staircases interwoven in random order. Each
subject participated in at least four test sessions.
2.4. Procedure
3. Results
In the first session, 18 Hz heterochromatic flicker
photometry was used to equate the intensity of the blue
and green phosphors to the red phosphor. The stimulus
was a 0.64°–2.77°. annulus surrounding a central fixation cross, and coincided with the four positions of IRF
test stimuli. Practice was provided in free view before
formal testing using the bite-bar. Because ocular media
transmission of the red phosphor is affected negligibly
3.1. Derivation of the impulse response
Fig. 1 shows log contrast plotted as a function of
ISI for a young observer (18.8 years). Insets illustrate
the theoretical relations between thresholds and the
impulse response. It is assumed that each stimulus pulse
elicits a response that may be approximated by an
0.16
Threshold Elevation
Log Contrast
0.14
0.12
0.10
0.08
0.06
0.04
Lowest Threshold
Threshold
Decrement
0.02
0.00
ISI (msec)
Fig. 1. Central panel shows log contrast threshold as a function of ISI. Insets show the theoretical manner in which threshold varies due to the phase
relations of the responses generated by each pulse pair.
620
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
exponentially-damped oscillation. The temporal separation between the stimuli will influence threshold. For
example, at the shortest ISI, the two responses will be
nearly in phase and summation will result in low contrast threshold. At higher temporal separation, when the
responses are out of phase, there is interference between
excitatory and inhibitory phases of the two responses so
threshold will be elevated. With further separation between pulses, interference will be reduced so threshold
will fall, albeit not to the extent of the first case because
summation of responses is incomplete.
Following Burr and Morrone (1993), we calculated
IRFs from the threshold data using the following
equation for an exponentially damped frequency-modulated sine wave:
IðtÞ ¼ a0 H ðtÞt sinf2p½a1 tðt þ 1Þ
a2
g expð
a3 tÞ;
ð1Þ
where IðtÞ is the impulse response as a function of time
ðtÞ, parameters a0–3 are positive with a0 defining the
overall gain, a1 the fundamental frequency of oscillation, a2 the modulation frequency over time, and a3 the
steepness of the decay. H ðtÞ is the Heaviside function to
assure that IðtÞ begins with a value of 0 when t < 0.
Thus,
H ðtÞ ¼ 0;
t < 0;
H ðtÞ ¼ 1;
t P 0:
The model was fitted to the data by varying four parameters, a0–3 , using a least-squares criterion. We chose
this model because it has fewer free parameters than
other models of the impulse response and does not require the unproven assumption that the impulse response derives from a minimum-phase filter (Watson,
1982; Swanson, Ueno, Smith, & Pokorny, 1987;
Uchikawa & Yoshizawa, 1993). That assumption can be
included, however, by using a2 ¼ 0, but we found that
this had little effect on the derived IRF in most cases.
For 19 of 70 observers, the value of a2 was more than
35% of minimum values of a0 , a1 , and a3 . But in 15 of
these subjects, the difference in fits between a2 ¼ 0 vs.
a2 6¼ 0 was negligible. Monophasic, biphasic and triphasic IRFs can be described with changing values of
a0–3 , and without a priori assumptions about the number
of lobes in the IRF.
The fitted functions are based on a model of probability summation of visual response (Watson, 1979),
Rðt; sÞ:
Rðt; sÞ ¼ K½IðtÞ þ H ðt sÞIðt sÞ;
ð2Þ
where s is the SOA (ISI is (s-[pulse duration])) and H ðtÞ
is the Heaviside function. K is the luminance of each
pulse over the background luminance and p, proportion
correct, is:
Z T
b
p ¼ 1 ð1 rÞ exp ð3Þ
j Rðt; sÞj dt ;
0
parameter r is the probability due to chance (0.25 in this
experiment) and parameter b, which determines the
steepness of the psychometric function, was set to 4. T is
the time to take the integral and must be long enough so
that all response will be zero within ISIs. We set T as
3.18
p s. P0 , the proportion correct at threshold, was
ð 2Þ=2, which is determined by the two-down one-up
procedure in the 4AFC method we employed. From
Eqs. (2) and (3), we obtained Eqs. (4) and (5) as:
!
" ,(
2385
X
b
K¼ C
jIðnDtÞ þ H ðnDt sÞIðnDt sÞj
n¼0
)#1=b
Dt
;
ð4Þ
ðLog contrast at thresholdÞ ¼ log10 ðð10 þ KÞ=10Þ; ð5Þ
p
where C is ln½ðp0 1Þ=ðr 1Þ (¼ lnðð4 2 2Þ=3Þ)
and Dt was set to 1.333 ms. n was changed from 0 to
2385 (3.18 s). In the model fit, parameters of the IRF
(a0 –a3 ) were changed to obtain the best fit to threshold
data points for each ISI using a least-squares method.
The left panel of Fig. 2 shows log contrast threshold
plotted as a function of ISI for typical younger (18.8
years) and older (60.2 years) observers. As expected,
thresholds are higher for the older observer. This was
confirmed for the entire sample by linear regression
analyses. Two-pulse contrast thresholds increased significantly with age for each of the 13 ISIs (p < 0:001).
The IRFs computed from the data of these two observers are presented in the right panel of Fig. 2. The
first and second phases of the IRF are interpreted as
excitatory and inhibitory phases, respectively. The
younger observer in this figure has a higher first-phase
amplitude, but does not differ from the older observer in
response timing for this phase. The younger observer
also has a faster second (inhibitory) phase. Overall, excitatory amplitude and timing parameters were not
correlated across observers, except for certain elderly
observers as defined in Section 3.3.
Because phase is lost in the double-pulse method, it
was occasionally found that two very different IRFs
could be fitted about equally well. In those cases, we
selected the IRF that was closest to the mean because
the shape of the other IRF always looked unrealistic
(e.g., low amplitude of excitation with high amplitude
of inhibition) relative to physiological measures.
3.2. Individual differences: trimodal impulse response
functions
The IRF was characterized by initial excitatory and
inhibitory phases, but for some observers the IRF was
trimodal due to a second excitatory phase. Fig. 3 shows a
trimodal IRF from a 37-year-old observer. In this example,
there is even a fourth phase (second inhibitory phase) with
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
0.20
621
1.5
0.18
1.0
0.16
Relative Response
Log Contrast
0.14
0.12
0.10
0.08
0.06
0.5
0.0
-0.5
0.04
-1.0
0.02
0.00
-1.5
0
50
100
150
200
0
50
ISI (msec)
100
150
200
Time (msec)
Fig. 2. Left panel shows contrast thresholds and model fits plotted as a function of ISI for two observers: open symbols and dashed curve, age 18.8
years; closed symbols and solid curve, age 60.2 years. Error bars denote 1 SEM. Right panel shows IRFs calculated from Eq. (1) for the same two
observers with dashed and solid curves as in the left panel.
0.20
1.5
0.18
1.0
0.16
Relative Response
Log Contrast
0.14
0.12
0.10
0.08
0.5
0.0
-0.5
0.06
0.04
-1.0
0.02
0.00
-1.5
0
50
100
150
200
ISI (msec)
0
50
100
150
200
Time (msec)
Fig. 3. Left panel shows contrast thresholds and model fits plotted as a function of ISI for a 37.0-year-old observer. Error bars denote 1 SEM.
Right panel shows the corresponding IRF calculated from Eq. (1).
low amplitude. Overall, IRFs with at least three phases
were obtained for 32 of the 70 observers. There tended to
be fewer trimodal functions among the older observers,
although this may have been secondary to a generalized
loss of inhibition as described in the next section.
3.3. Individual differences: inhibitory phase
Fig. 4 shows data and model fits for a 71.6-year-old
observer. Note that the amplitude of the inhibitory
phase of the IRF is low. The excitatory phase is thus
slow and long. A reduced inhibitory phase (to <20% of
the absolute value of the excitatory phase) was found in
17 observers. Subjects with reduced inhibitory phase
could be observed from age 26 years, after which their
proportion was stable until about 60, but the proportion
rapidly increased with age after about 60 years. Additionally, six other observers demonstrated near-zero
inhibitory phase. The near absence of inhibitory phase
was found only for observers above the age of 70 years.
622
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
1.5
0.20
0.18
1.0
0.16
0.14
Relative Response
Log Contrast
0.5
0.12
0.10
0.08
0.0
-0.5
0.06
0.04
-1.0
0.02
0.00
-1.5
0
50
100
150
0
200
50
ISI (msec)
100
150
200
Time (msec)
Fig. 4. Left panel shows contrast thresholds and model fits plotted as a function of ISI for a 71.6-year-old observer. Error bars denote 1 SEM.
Right panel shows corresponding IRF calculated from Eq. (1).
3.4. Control for optical factors
The contrast thresholds from the three pseudophakic
observers were in agreement with that of their agematched cohorts as will be shown in subsequent figures
and as might be expected with our procedures that essentially equate retinal illuminance across observers.
Subjects were refracted for the test distance and our
conditions were chosen to be insensitive to blur and small
fixation inaccuracies, as the stimuli were large and spatially tapered by a Gaussian envelope. In addition, the
effective pupil diameter of 2.5 mm helps to maintain contrast sensitivity across spatial frequencies that would otherwise decline with the introduction of optical aberrations
and optical defocus (Green & Campbell, 1965; Charman,
1979). As a control, however, we tested two observers
(ages 29 and 38 years) with and without 1.0–1.5 D of
positive defocus. Contrast thresholds were measured for
all ISIs over several sessions for each observer. The results
of the induced blur condition differed negligibly from that
obtained under our standard conditions. Individual and
age-related changes in the IRF under these conditions,
therefore, are not attributable to optical factors.
in relation to age. Fig. 5 shows the peak amplitude of the
first phase of the IRF for 70 phakic and three pseudophakic observers (XÕs) plotted as a function of age. A
regression analysis based on all phakic observers showed
that there is a significant reduction in first-phase amplitude with age (r ¼ 0:53; F1;68 ¼ 24:600, p < 0:001).
Fig. 6 shows the change in inhibitory amplitude of the
IRF plotted as a function of age. The regression line
indicates a significant reduction in inhibitory amplitude
with increasing age (r ¼ 0:46; F1;69 ¼ 7:951, p < 0:01). A
number of the older observers had a complete loss of
inhibitory phase as is evident from examination of the
1.4
Positive Peak Amplitude (relative units)
In observers over 70, who have little or no inhibitory
phase, six were male and seven were female. Overall,
there was no significant difference in the proportion of
males and females with reduced or near-absent IRF
inhibition.
1.2
1.0
0.8
0.6
0.4
0.2
0.0
10
20
30
40
50
60
70
80
90
Age (years)
3.5. Senescent changes in the impulse response
Individual differences in the IRF are substantial so a
large group of observers is required to evaluate changes
Fig. 5. Amplitude of the first (positive, excitatory) phase of the IRF is
plotted as a function of age. The regression line was fitted to the data
of all (phakic) observers denoted by filled symbols. XÕs denote
pseudophakic observers.
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
623
0.0
Time to Positive Peak (msec)
Negative Peak Amplitude (relative units)
50
-0.2
-0.4
-0.6
10
20
30
40
50
60
70
80
20
10
10
Age (years)
20
30
40
50
60
70
80
90
Age (years)
Fig. 7. Time to peak of the first (positive, excitatory) phase of the IRF
is plotted as a function of age. The regression line was fitted to the data
of all observers denoted by filled symbols. XÕs denote pseudophakic
observers.
90
80
Positive Phase Duration (msec)
figure and this causes a ceiling effect that reduces the
strength of the correlation. Overall, it is clear that the
two primary phases of the IRF undergo a significant loss
in amplitude with increasing age, and that some elderly
observers exhibit a complete loss of IRF inhibition.
In contrast to amplitude, response timing of the excitatory phase is stable across the age range of our observers. This is shown in Fig. 7. The slope of the
regression line is not statistically significant. The analysis of the duration of the first excitatory phase is more
complicated due to observers with little or no inhibitory
phase. For those observers with a loss of inhibition
(Section 3.3), the duration of excitation necessarily increases. To provide a clearer evaluation of possible agerelated changes, least-squares linear regression lines in
Fig. 8 are presented for the overall group and after removing observers with little inhibitory amplitude (<20%
of the absolute value of the excitatory phase) or no inhibitory phase, denoted by triangles and squares, respectively. For the latter observers, the duration of the
excitatory phase steadily increased with age and the
slope of the regression line is significant (F1;21 ¼ 23:921,
p < 0:0001). This is shown in Fig. 8 by the dashed line.
These observers are responsible for a significant increase
in the duration of the positive phase of the IRF for the
overall group (F1;68 ¼ 18:988, p < 0:0001), shown by the
bold solid line. When observers with little or no inhibition are excluded, as shown by the thin solid regression
line, there is no significant change with age. For this
group, the duration of the first excitatory phase of the
IRF was 40–60 ms, regardless of age (intercept of the
regression line ¼ 46.6 ms). Thus, for the majority of
observers, the excitatory phase has stable temporal
characteristics with age, while for some observers there
30
0
90
Fig. 6. Amplitude of the second (negative, inhibitory) phase of the
IRF is plotted as a function of age. Regression line was fitted to the
data of all observers denoted by filled symbols. XÕs denote pseudophakic observers.
40
70
60
50
40
30
20
10
20
30
40
50
60
70
80
90
Age (years)
Fig. 8. Duration of the first (positive, excitatory) phase of the IRF is
plotted as a function of age. Bold regression line was fitted to all
phakic observers. XÕs denote pseudophakic observers. Filled circles
and thin solid regression line represents phakic observers except for
those with little (M) or no () inhibitory amplitude. The dashed regression line was fitted based on the latter observers.
is a change secondary to the loss of inhibitory amplitude.
Fig. 9 shows the peak time for the inhibitory phase of
the IRF plotted as a function of age using the same
plotting conventions as in Fig. 8. The thin solid line
fitted to phakic observers, except for those with little
inhibitory amplitude, is not statistically significant, indicating that the time to the peak of the inhibitory
IRF was essentially constant (intercept ¼ 65.89 ms). For
observers with little inhibitory amplitude, a separate
624
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
71 observers ranging in age from 9 to 80 years. The
kernel series was used to synthesize a single-flash response (Sutter, 2000). The mfERG results are remarkably similar to the psychophysical results presented in
this paper. The retinal IRF demonstrated significant
reductions in amplitude (response density), but not speed
(implicit time) with age. These findings support the interpretation that some of the loss in psychophysical IRF
may be due to changes in the outer retina. None of the
IRFs obtained with the mfERG were triphasic, however. This component of the psychophysical IRF may
be derived from processes beyond the retina.
Time to Negative Peak (msec)
110
100
90
80
70
60
50
40
4.1. Trimodal IRFs and possible sites of senescent changes
30
10
20
30
40
50
60
70
80
90
Age (years)
Fig. 9. Time to peak of the second (negative, inhibitory) phase of the
IRF is plotted as a function of age. Symbols and regression lines as in
Fig. 8.
regression shows that there is a significant increase in the
time to the peak inhibitory phase (F1;15 ¼ 12:988, p <
0:01) as can be seen from the dashed line. This subset of
observers is responsible for a modest but significant
increase among the overall group of phakic subjects
indicated by the bold regression line in Fig. 9 (F1;62 ¼
7:314, p < 0:01).
4. Discussion
The results of this research demonstrate that there are
significant reductions in the amplitude of both the excitatory and inhibitory phases of the IRF. For some
observers, there is a dramatic loss of inhibitory phase
(<20% of the excitatory phase). Those observers with no
inhibitory phase are only found among the elderly (>70
years). When those observers are excluded from analyses
of the timing of the IRF, there is no significant change in
relation to age for either the positive or negative phases
of the IRF.
In our previous work, we have shown that much of
the senescent sensitivity loss in cone pathways is due to
early changes in the stream of processing, mathematically equivalent to reduced quantal efficiency or elevations in neural noise (Schefrin, Werner, Plach, & Utlaut,
1992; Schefrin, Shinomori, & Werner, 1995). Senescent
changes in additive neural noise have not been found for
an M-/L-cone pathway (Werner, Schelble, & Bieber,
2001), but a change in the IRF amplitude might result,
at least in part, from the sensitivity losses in cone
pathways that occur with age.
In a parallel study in our laboratory (Gerth, Sutter, &
Werner, 2002), a retinal IRF was extracted from the
multifocal electroretinogram (mfERG) obtained from
Nearly half (46%) of our observers demonstrated
triphasic IRFs. Trimodal impulse response functions
have been reported for some observers by Kim and
Mayer (1994) who derived their IRFs from tCSFs.
Triphasic IRFs have also been inferred under suprathreshold conditions with pairs of intense brief (5 ms)
flashes (Bowen, 1989) and for luminance modulated
patterns during saccades (Burr & Morrone, 1996). The
importance of the number of phases in the IRF was
examined by Stork and Falk (1987) through modeling of
KellyÕs (1961) tCSFs obtained with large fields (60°).
They show that the more narrow the bandpass of a
tCSF, the more oscillations inherent in the corresponding IRFs. When the triphasic function is reduced
to a biphasic function in modeling, it results in a calculated tCSF that is in error by as much as 50% at low
temporal frequencies implying that multiple oscillations
of the IRF are not an artifact of modeling. Stork and
Falk found that multiple oscillations of the IRF were
most evident in KellyÕs data measured at 77 Trolands,
which is similar to the retinal illuminance of this study
(49 Td.).
Trimodal IRFs can also be seen in the membrane
current response of some primate cones, although they
are more typically diphasic (Schnapf, Nunn, Meister, &
Baylor, 1990). A trimodal response is not typically reported for P-cells, but is seen for M-cells at higher
contrasts (Lee, Pokorny, Smith, & Kremers, 1994). Benardete (1994) reported trimodal IRFs in M ON cells, in
response to achromatic, low spatial frequency stimuli,
but not with high spatial frequency patterns. Our achromatic increments presented on an achromatic background are consistent with the conditions in which
Benardete found trimodal impulse response functions
from primate M-cells. It seems likely that M-cells are
responsible for detection of the stimuli in this experiment because of their larger receptive fields and higher
contrast sensitivity compared to P-cells (Kaplan &
Shapley, 1986). In this context, it is worth noting that
age-related changes in an M-cell pathway have been
inferred from senescent changes in scotopic contrast
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
sensitivity under conditions in which only M-cells are
likely to be sensitive (Schefrin, Tregear, Harvey, &
Werner, 1999). It is possible that the changes in the IRF
demonstrated here are due, in part, to changes in an
M-cell pathway.
4.2. Slower IRFs with reduced or near-zero inhibitory
phase
As described in Section 3.5, the time to the peak of
the IRF is nearly constant for all observers, but the
duration of the positive phase of the IRF is necessarily
longer for observers with reduced inhibitory phase. This
is inherent in the antagonistic relation between excitation and inhibition; reduced inhibition causes the crossover to shift toward higher first-phase duration. The loss
of IRF inhibition in some elderly observers could be due
to (1) an overall reduction in signal strength and/or (2) a
specific loss of inhibition.
Stork and FalkÕs analyses demonstrate that with reduced retinal illumination, there is a reduction in inhibitory phase and a loss of higher-order oscillations in
the IRF. The stimuli used in this study were essentially
equated for retinal illuminance, but they may nevertheless have been less effective for older observers due to
reduced sensitivity of cone pathways. The inhibitory
amplitude of the IRFs derived in this study may have
been more stable across age if the stimuli were initially
equated with respect to increment threshold.
The site of inhibitory loss in some older observers
could occur in an M-cell pathway as already mentioned,
but it could also involve a change in low-pass filtering
mechanisms in the cortex (Lee, Pokorny, Smith, Martin,
& Valberg, 1990). This suggestion is buttressed by simultaneous recordings of pattern electroretinograms
(pERG) and visually evoked potentials (VEPs) in young
and elderly observers by Porciatti, Burr, Morrone, and
Fiorentini (1992). They concluded that at least some of
the loss in temporal response with age is due to changes
at post-retinal sites.
Senescent loss of inhibition in the spatial domain has
been demonstrated through single-unit recordings in
primary visual cortex of elderly rhesus macaque monkeys
(Schmolesky, Wang, Pu, & Leventhal, 2000). Specifically,
elderly animals had decreased orientation and direction
selectivity and these changes appear not to be secondary
to changes at precortical sites (Spear, Moore, Kim, Xue,
& Tumosa, 1994). Thus, while the senescent reduction in
the overall amplitude of the IRF may occur at a retinal
stage, the specific loss in the inhibitory phase could be
mediated at more central sites of temporal processing.
4.3. Implications for temporal contrast sensitivity
For a linear system, the impulse response is directly
related to the tCSF by the inverse Fourier transform.
625
Burr and Morrone (1993) calculated tCSFs from their
two-pulse data using Eq. (1) and found that they predicted the shape of empirically-determined tCSFs measured with counterphase sinusoidal gratings. Several
previous studies of age-related change in temporal vision
have derived a theoretical IRF based on measured
tCSFs for younger and older observers (Tyler, 1989;
Kim & Mayer, 1994), but not the other way around.
Theoretical tCSFs were calculated for younger (20
years) and older (80 years) observers of this study. The
latter were generated for older observers with normal
age-related losses in inhibition or a complete loss of
inhibitory IRF amplitude. These tCSFs were generated
from theoretical IRFs calculated using six parameters
from the regression lines fitted to the data: (1) positive
peak amplitude (Fig. 5), (2) negative peak amplitude
(Fig. 6), (3) time to positive peak (Fig. 7), (4) duration of
the positive phase (Fig. 8), (5) time to negative peak
(Fig. 9), and (6) second zero crossing time (i.e., combined duration of the first positive and negative phases;
not shown in figures). From Eq. (1) a set of a0 –a3 parameters was calculated such that the theoretical IRFs
agreed with the six empirical constraints based on leastsquares criteria. The resultant theoretical IRFs are
shown by the inset in Fig. 10.
A fast Fourier transform of the theoretical IRFs was
calculated to obtain theoretical tCSFs (MATLAB v. 6.1,
The MathWorks, Inc., Natick, MA). To minimize the
assumptions inherent in this computation (Dagnelie,
1992), we also calculated a discrete convolution of the
IRF and sinusoidal stimulus modulation in 13.3–1.11 ms
steps (0.5–80 Hz in the frequency domain). Temporal
contrast sensitivity was defined by the output-signal
contrast at the stable portion of the convolution (i.e.,
when the amplitude of the IRF was less than 1% of the
maximum or minimum to avoid phase-dependent stimulus transients). Error associated with this approximation is 3%. The resultant tCSFs are shown in Fig. 10
for each type of observer. As expected from the shape of
the IRFs, the theoretical tCSF of the older observer with
IRF inhibition has the same shape as the younger observer, but overall sensitivity is lower. These functions
are consistent with previously reported data (Kim &
Mayer, 1994; Tyler, 1989). The theoretical tCSF of the
older observer lacking IRF inhibition is quite different.
It has a low-pass shape with reduced sensitivity at
middle- and higher temporal frequencies; at frequencies
below 3 Hz, the predicted sensitivity of the older observer with no inhibitory amplitude is higher than for
the older cohort and is similar to that of a younger
observer. The reduction of inhibitory phase of this older
theoretical observer is consistent with longer integration
of cone signals and reduced temporal resolution. Older
observers with low-pass tCSFs have not been reported,
presumably because previous studies have not used
stimuli below 1.5 Hz and the luminance levels used in
626
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
Fig. 10. Temporal contrast sensitivity functions (tCSFs) for theoretical 20-year-old (thin smooth curve) and 80-year-old observers with
normal or no second phase (inhibitory) amplitude. Log contrast sensitivity in relative units is plotted as a function of temporal frequency.
Inset: The theoretical IRFs used to generate these tCSFs calculated
from Eq. (1). Curves are plotted as in the main figure.
previous studies were substantially higher than in the
present study. Overall, the IRFs and theoretical tCSFs
of this study are consistent with the conclusion of Kim
and Mayer (1994) that senescent changes in temporal
processing primarily involve sensitivity, not resolution.
This follows from the relatively stable temporal characteristics of the IRF for most observers, but a senescent
reduction in IRF amplitude.
Acknowledgements
We gratefully acknowledge the assistance of Susan
Garcia, and the comments of Charlene B.Y. Kim and
William H. Swanson. This study was funded by the
High-Tech Research Center Development Program (by
the Ministry of Education, Culture, Sports, Science and
Technology, Japan), the Mitsui-Sumitomo Insurance
Welfare Foundation, the National Institute on Aging
(grant AG04058), the National Eye Institute (CORE
grant EY12576) and a Jules and Doris Stein Professorship from Research to Prevent Blindness.
References
Benardete, E. A. (1994). Functional dynamics of primate retinal
ganglion cells. Ph.D. dissertation, The Rockefeller University,
New York.
Bowen, R. W. (1989). Two pulses seen as three flashes: A superposition
analysis. Vision Research, 29, 409–417.
Burr, D. C., & Morrone, M. C. (1993). Impulse-response functions for
chromatic and achromatic stimuli. Journal of the Optical Society of
America A, 10, 1706–1713.
Burr, D. C., & Morrone, M. C. (1996). Temporal impulse response
functions for luminance and colour during saccades. Vision
Research, 36, 2069–2978.
Charman, W. N. (1979). Effect of refractive error in visual tests with
sinusoidal gratings. British Journal of Optometry, 33, 10–20.
Coppinger, N. W. (1955). The relationship between critical flicker
frequency and chronologic age for varying levels of stimulus
brightness. Journals of Gerontology, 10, 48–52.
Dagnelie, G. (1992). Temporal impulse responses from flicker sensitivities: practical considerations. Journal of the Optical Society of
America A, 9, 659–672.
DeLange, H. (1958). Research into the dynamic nature of the human
fovea––cortex systems with intermittent and modulated light. I.
Attenuation characteristics with white and colored light. Journal of
the Optical Society of America, 48, 777–784.
Gerth, C., Sutter, E. E., & Werner, J. S. (2002). The impulse response
of the aging retina. Association for Research in Vision and
Ophthalmology, Fort Lauderdale, FL, 6 May 2002 (Abstract).
Green, D. G., & Campbell, F. W. (1965). Effect of focus on the visual
response to a sinusoidally modulated spatial stimulus. Journal of
the Optical Society of America, 55, 1154–1157.
Ikeda, M. (1965). Temporal summation of positive and negative
flashes in the visual system. Journal of the Optical Society of
America, 55, 1527–1534.
Kaplan, E., & Shapley, R. M. (1986). The primate retina contains two
types of ganglion cells, with high and low contrast sensitivity.
Proceedings of the National Academy of Sciences of the United
States of America, 83, 2755–2757.
Kelly, D. H. (1961). Visual responses to time-dependent stimuli. I.
Amplitude sensitivity measurements. Journal of the Optical Society
of America, 51, 422–429.
Kim, C. B. Y., & Mayer, M. J. (1994). Flicker sensitivity in healthy
aging eyes. II. Cross-sectional aging trends from 18 through 77
years of age. Journal of the Optical Society of America A, 11, 1958–
1969.
Kline, D., & Scheiber, H. (1982). Visual persistence and temporal
resolution. In R. Sekuler, D. Kline, & K. Dismukes (Eds.), Aging
and human visual function (pp. 231–244). New York: A.R. Liss, Inc.
Kuyk, T. K., & Wesson, M. D. (1991). Aging-related foveal flicker
sensitivity losses in normal observers. Optometry and Vision
Science, 68, 786–789.
Lee, B. B., Pokorny, J., Smith, V. C., & Kremers, J. (1994). Responses
to pulses and sinusoids in macaque ganglion cells. Vision Research,
34, 3081–3096.
Lee, B. B., Pokorny, J., Smith, V. C., Martin, P. R., & Valberg, A.
(1990). Luminance and chromatic modulation sensitivity of
macaque ganglion cells and human observers. Journal of the
Optical Society of America A, 7, 2223–2236.
Loewenfeld, I. E. (1979). Pupillary changes related to age. In H. S.
Thompson, R. Daroff, L. Frisen, J. S. Glaser, & M. D. Sanders
(Eds.), Topics in neuro-ophthalmology (pp. 124–150). Baltimore:
Williams and Wilkens.
Mayer, M. J., Kim, C. B. Y., Svingos, A., & Glucs, A. (1988). Foveal
flicker sensitivity in healthy aging eyes. I. Compensating for pupil
variation. Journal of the Optical Society of America A, 5, 2201–
2209.
Porciatti, V., Burr, D. C., Morrone, C., & Fiorentini, A. (1992). The
effects of ageing on the pattern electroretinogram and visual evoked
potential in humans. Vision Research, 32, 1199–1209.
Rashbass, C. (1970). The visibility of transient changes of luminance.
Journal of Physiology, 210, 165–186.
Schefrin, B. E., Shinomori, K., & Werner, J. S. (1995). Contributions
of neural pathways to age-related losses in chromatic discrimination. Journal of the Optical Society of America A, 12, 1233–1241.
K. Shinomori, J.S. Werner / Vision Research 43 (2003) 617–627
Schefrin, B. E., Tregear, S. J., Harvey, L. O., Jr., & Werner, J. S.
(1999). Senescent changes in scotopic contrast sensitivity. Vision
Research, 39, 3728–3736.
Schefrin, B. E., Werner, J. S., Plach, M., & Utlaut, N. (1992). Sites of
age-related sensitivity loss in a short-wave cone pathway. Journal of
the Optical Society of America A, 9, 355–363.
Schmolesky, M. T., Wang, Y., Pu, M., & Leventhal, A. G. (2000).
Degradation of stimulus selectivity of visual cortical cells in
senescent rhesus monkeys. Nature Neuroscience, 3, 384–390.
Schnapf, J. L., Nunn, B. J., Meister, M., & Baylor, D. A. (1990).
Visual transduction in cones of the monkey Macaca Fascicularis.
Journal of Physiology, 427, 681–713.
Spear, P. D., Moore, R. J., Kim, C. B. Y., Xue, J., & Tumosa, N.
(1994). Effects of aging on the primate visual system: spatial and
temporal processing by lateral geniculate neurons in young and old
rhesus monkeys. Journal of Neurophysiology, 72, 402–420.
Stork, D. G., & Falk, D. S. (1987). Temporal impulse responses from
flicker sensitivities. Journal of the Optical Society of America A, 4,
1130–1135.
Sutter, E. E. (2000). The interpretation of multifocal binary kernels.
Documenta Ophthalmologica, 100, 49–75.
Swanson, W. H. (1993). Chromatic adaptation alters spectral sensitivity at high temporal frequencies. Journal of the Optical Society of
America A, 10, 1294–1303.
Swanson, W. H., Fiedelman, M., & Fish, G. E. (1995). Flicker
sensitivity in patients with retinitis pigmentosa and good acuity. In
1995 technical digest series: Vol. 1. Vision science and its applications (pp. 292–295). Washington, DC: Optical Society of America.
Swanson, W. H., Ueno, T., Smith, V. C., & Pokorny, J. (1987).
Temporal modulation sensitivity and pulse-detection thresholds for
chromatic and luminance perturbations. Journal of the Optical
Society of America A, 4, 1992–2005.
627
Tyler, C. W. (1989). Two processes control variations in flicker
sensitivity over the life span. Journal of the Optical Society of
America A, 6, 481–490.
Uchikawa, K., & Yoshizawa, T. (1993). Temporal responses to
chromatic and achromatic change inferred from temporal doublepulse integration. Journal of the Optical Society of America A, 10,
1697–1705.
Victor, J. D. (1989). Temporal impulse responses from flicker
sensitivities: causality, linearity, and amplitude data do not
determine phase. Journal of the Optical Society of America A, 6,
1302–1303.
Watson, A. B. (1979). Probability summation over time. Vision
Research, 19, 515–522.
Watson, A. B. (1982). Derivation of the impulse response: comments
on the method of Roufs and Blommaert. Vision Research, 22,
1335–1337.
Watson, A. B., & Nachmias, J. (1977). Patterns of temporal integration in the detection of gratings. Vision Research, 17, 893–902.
Weale, R. A. (1982). A biography of the eye. London: H. K. Lewis &
Co., Ltd.
Weale, R. A. (1988). Age and the transmittance of the human
crystalline lens. Journal of Physiology, 395, 577–587.
Werner, J. S. (1982). Development of scotopic sensitivity and the
absorption spectrum of the human ocular media. Journal of the
Optical Society of America, 72, 247–258.
Werner, J. S., Schelble, K. A., & Bieber, M. L. (2001). Age-related
increases in photopic increment thresholds are not due to an
elevation in intrinsic noise. Color Research and Application, 26, 48–
52.
Wright, C. E., & Drasdo, N. (1985). The influence of age on the spatial
and temporal contrast sensitivity function. Documenta Ophthalmologica, 59, 385–395.