DAILY RHYTHM OF TEMPORAL RESOLUTION
IN THE AUDITORY SYSTEM
Martin Lotze, Marc Wittmann, Nicole von Steinbüchel, Ernst Pöppel
and Till Roenneberg
(Institut für Medizinische Psychologie, Ludwig-Maximilians-Universität, München,
Germany)
ABSTRACT
Over a period of 24 hours, fusion thresholds (click durations 100 µs) were assessed in 7
subjects. Over the same period, order thresholds (click duration of 1 ms) were measured in
10 subjects (12 independent sessions). Auditory fusion thresholds showed a diurnal rhythm
with a maximum performance (shortest intervals) around midnight. In contrast, order
thresholds appear to be independent on the time of day. Sex specific differences in threshold
levels were only observed in order thresholds but not in fusion thresholds.
Key words: diurnal rhythm, temporal resolution thresholds, order threshold, acoustic,
sex difference
INTRODUCTION
When subjects are presented two clicks with an inter-stimulus-interval (ISI)
in the range of a few milliseconds, the perception of their sequence may differ
from their real order. At least two temporal thresholds can be assessed, which
shows that information processing is submitted to certain temporal constraints of
the processing system (Pöppel, 1989; for a discussion of threshold models see
Ulrich, 1987, and Jaskowski, 1991). At the most basic threshold (Fusion
threshold = FT), two clicks are perceived as one. Thus, fusion thresholds
separate the impression of simultaneity and non-simultaneity. They are assessed
by presenting two stimuli with decreasing ISIs until the subject perceives only
one. FTs are specific for the tested sensory modality, probably due to different
transduction times (Hirsh and Sherrick, 1961; Pöppel, 1989; Pöppel and
Steinbüchel v., 1998; for a detailed description on the physiology of transduction
times, see Torre, Ashmore, Lamb et al., 1995): with stimulus durations of 1 ms,
tactile FTs in normal subjects lie around 10 ms, visual FTs around 20 ms. For a
recent review on temporal resolution in different sensory modalities see Artieda
and Pastor (1996).
Auditory fusion thresholds lie between 1 and 3 ms (Lackner and Teuber,
1973; Hosokawa, Nakamura and Shibuya, 1981). This relatively large range is
due to methodological differences (e.g., duration of the clicks or different slopes
of the clicks’ ramps).
Even when subjects perceive two clicks to be non-simultaneous, they are not
Cortex, (1999) 35, 89-100
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able to state their correct temporal sequence below the order threshold (OT). For
click durations of 1 ms, healthy subjects detect the correct order of two stimuli
(i.e., can state correctly whether the right or the left stimulus was the first of the
pair) at ISIs above 20 to 40 ms (Hirsh, 1959; Steinbüchel v., 1995). Unlike the
FT, the OT appears to be independent of sensory modality (Hirsh and Sherrick,
1961). This fact has lead to the hypothesis, that central, receptor independent
mechanisms are responsible for the identification of temporal order (Pöppel,
1997; Pöppel and Steinbüchel v., 1998).
Experiments establishing the OT under different conditions and for different
sensory modalities have provided insights into a number of fundamental issues
in information processing, e.g., attentional influences on perceptual processing
(Sternberg and Knoll, 1973; Jaskowski, 1993; Gibson and Egeth, 1994). In
experiments establishing auditory thresholds, clinical evidence was gained that
the neuronal mechanisms involved in temporal processing are localized in the
left hemisphere and are often closely related to the processing of speech. OTs
are two fold increased in aphasic patients with left hemispheric damages in the
posterior region (Swisher and Hirsh, 1972; Steinbüchel v., Wittmann and Pöppel,
1996), while the FTs are only moderately higher or unchanged in these patients
(Lackner and Teuber, 1973). When aphasic patients are trained in the detection
of temporal order, OTs can be reduced to the values of healthy subjects
(Steinbüchel v. and Pöppel, 1991; Steinbüchel v., 1995; Steinbüchel v. et al.,
1996). Along with the decreased OTs, improved phoneme discrimination is
achieved. This points to the importance of temporal order in speech perception.
Several psychophysical variables, such as reaction time, calculation velocity,
auditory and visual sensitivity, depend on time of day. Most of these “diurnal
rhythms” depend on vigilance. For example, the performance in tasks such as
reaction times in all modalities, speed of computation, visual flicker fusion
(Schulz, Weyer, Jobert et al., 1992), and visual double-pulse resolution (Lotze,
1996) show maximum performance in the afternoon around 2 p.m. At this time,
subjects also produce the shortest intervals in time production tests (subjects
were instructed to press a button for the duration of 10 seconds), indicating an
accelerated internal oscillating mechanism compared to other times of day
(Pöppel and Giedke, 1970). Other psychophysical functions do not depend on
central vigilance but on peripheral changes in sensory organs. For example,
visual sensitivity to white light (Knoerchen and Hildbrandt, 1976; Bassi and
Powers, 1986), to colored light stimuli (Roenneberg, Lotze and Steinbüchel,
1992) as well as to acoustic stimuli (Lotze, 1996) show a diurnal rhythm that is
dependent on changes in the sensory organ. In the visual system, these changes
have been correlated to changes in morphology and in mechanisms of the
receptor organ (Remé, Wirz-Justice, Rhyner et al., 1986). These sensorydependent rhythms oscillate counter-phasic, i.e., with a temporal phase
difference of 180° compared to vigilance dependent variables (maximum
performance after midnight around 2 a.m.).
With respect to the diagnosis of brain injured patients and their training in
auditory resolution (e.g., OT training), it is important to investigate the diurnal
time course of healthy subjects. Without this information, interpretations of
results gained in patients are difficult. We were interested whether FT and OT
24h changes in auditory temporal resolution
91
show a diurnal variation and if so whether it is of the vigilance- or sensorydependent type and investigated, therefore, the time course of FT and OT over
24 hours in constant conditions.
MATERIALS
AND
METHODS
Tests and Procedure
In all measurements (FTs and OTs) rectangular pulses (FT: clicks of 100 µs, OT: clicks
of 1 ms) produced by a “Hi-Med”-generator (except for the third series of OT
measurements) were amplified (Akai 2250) and presented binaurally using headphones
(Bayer Monocor). For FT measurements, intensity on both sides was adjusted to 70 dB
SPL (sound pressure level). Although SPLs above 40 dB can lead to lateral cross-talk (the
acoustic stimulation of one ear also leads to sound detection by the contralateral ear), we
chose this SPL for two reasons. First, we wanted to compare our results with other published
FT and OT measurements which were performed with higher sound pressure levels,
secondly, low SPLs constitute high stress for the subjects during 24-hour experiments. In
addition, the aim of our experiments was the investigation of diurnal time courses in fusion
and order thresholds. Any cross-talk, therefore, constitutes a constant factor over the 24hour period and certainly could not explain any observed differences either between two
different time points or between the timecourses of the two measured thresholds. For OT
measurements, headphones were tuned for every subject, so that the same subjective
stimulus intensity (~ 70 dB SPL) was perceived in both ears. Stimuli (left or right ear first)
were presented in random order. Subjects were instructed to keep a strict sleep schedule
from midnight to 8 a.m. for the duration of one week before each experiment. Approximate
thresholds for each subject were determined on the day before the experiment.
Fusion Threshold (FT)
Fusion thresholds were measured by gradually decreasing ISIs by steps of 0.1 ms,
starting 5 ms above the expected threshold, until subjects reported the two signals to have
fused to one. Every test series consisted of two trials (left first, right first), lasting
approximately 5 min. Measurements were repeated every 2 h throughout the 24-h
experiment. Two identical 24 h tests were carried out. Three subjects participated in the
first test (one female, two males, age 27 to 31) which lasted from 8 a.m. to 9 a.m. the next
day. The second test started at 10 a.m. and continued until 11 a.m. the following day (two
female and two male subjects, age 24 to 29).
Order Threshold (OT)
To identify the individual stimuli, we chose binaural sequential stimulation, so that both
stimuli had identical acoustic properties and could only be identified spatio-temporally
(right or left first). This way, we excluded all other possible identification strategies. Three
different methods were used for OT measurements which are described in Table I. The first
method was chosen, because it is used in testing and training aphasic patients (Steinbüchel
v., 1995). However, in this method ISIs could only be changed in 10 ms steps which we
regarded to be insufficiently sensitive to detect the small OT differences expected in healthy
subjects. We therefore applied a second method allowing smaller steps (2 ms). The
procedural sequence of OT measurements followed a statistical method initially worked out
by Levitt (1970). In a third test, we used a statistically automated method less concerned
with trials far above or below the actual threshold. This procedure was modified (Treutwein
and Rentschler, 1992; Treutwein, 1997) based on the maximum likelihood method (Hall,
1968) and the Bayesian estimation (Emmerson, 1986). This method allowed to measure OT
differences in 1 ms steps. For a detailed methodological discussion on psychophysical
procedures see Treutwein (1995).
In all three experiments, the possible answers were: left (first), right (first) and
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TABLE I
Methods for Order Threshold Measurements
Specification
Test 1
Test 2
Test 3
Duration of
experiment
Measurements
per person
and experiment
Sex (f/m)
Age (years)
Stimuli were
presented...
Sep. 2 – Sep. 3
8 a.m. – 9 a.m.
12
Nov. 3 – Nov. 4
10 a.m. – 10 a.m.
10
Aug. 15 – Aug. 16
7 a.m. – 9 a.m.
16
2 at every time point
Thresholds were
defined...
Overall mean
threshold (ms)
1/1
27-31
in a down-staging
method always starting
at 50 ms (steps of 10
ms)
2/3
24-29
in a down-staging method
always starting at 30 ms
(steps of 2 ms)
when at least 4 of 5
click pairs were
recognized correctly
when the first wrong answer
was given. Thereafter,
ISIs were in- and decreased
in steps of 2 ms three times
above and below the correct
detection. The threshold was
defined at lowest ISI with
three pairs of correct
answers*
21 ± 4.5
24 ± 12.7
3/2
24-30
according to a computer
generated programm
based on the adaptive
ML-Bayes method **
(steps of 1 ms)
36.7 ± 10.5
Note. The two subjects of test 1 were also tested in test 2.
* Method developed by Levitt (1970).
** Method adopted from Bayes (see Emmerson, 1986) by Treutwein (1997).
simultaneous (always treated as incorrect). Again, test series were carried out every two
hours. In each of the test series, the OTs for different stimulus presentations (left or right
lead) were measured separately but the mean of the two values was used for future
evaluations. This was possible because no significant differences were found when the left
or the right ear received the first stimulus (data not shown). This lack of lateralization is in
contrast to the results reported by others (Mills and Rollman, 1980). In all three experiments
a total of 11 different healthy subjects (age 24 to 31) were tested, one of whom participated
in two different test methods (N = 12).
Data Analysis
For the calculation of the diurnal time course, thresholds (t) were expressed as deviation
(td) from the individual daily mean (tø) td = t – tø. Composite cosine curves (two harmonic)
were fitted to the data using the least squares method (Box and Jenkins, 1970), and the
correlation coefficients were used to estimate significance levels based on the χ2−test. The
phase of a diurnal rhythm was defined by using either the maximum or the minimum of
the cosine fit as reference point.
RESULTS
Fusion Threshold (FT)
FTs showed a large inter-individual variance with a total mean of 660 µs
(dashed line in Figure 1; N = 168 measurements). The sex-specific difference in
24h changes in auditory temporal resolution
93
the overall means (530 µs for males and 840 µs for females) is not statistically
significant. Mean values per time point (measurements for all subjects were
averaged within bins of 2 hours) show almost identical diurnal variation in both
tests (Figure 2). Standard deviations of individual means appeared to be larger
around noon, but consistent, time of day specific differences in the standard
deviations are not apparent across the two experiments. The composite cosine
fits indicate for both experiments a range of oscillation around 440 µs with two
times of maximum performances (shortest ISIs) around 8 p.m. and 6 a.m.,
respectively. Diurnal variations are highly significant in both experiments (r >
0.75; p ≤ 0.01; r > 0.87; p ≤ 0.001).
Order Threshold (OT)
The overall mean OT for all subjects including all three test methods, was
28.58 ms (range 15-48 ms). The means for the different test methods
show differences up to 15.7 ms (last row in Table I). Figure 3 shows the
Fig. 1 – Mean and standard deviations (vertical lines) of average fusion thresholds (FT) for each
subject grouped by sex (bars representing male subjects are filled gray). The over all mean (dashed
line) was 660 µs. Sex-specific means show no significant difference (Mann-Whitney U-test).
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Fig. 2 – Diurnal time course for fusion thresholds (FT): Mean (circles) and standard deviation
(vertical lines) of all subjects in test 1 (bottom and left ordinate) and test 2 (top and right ordinate).
Values represent means within 2-h-bins. Composite cosine fits (24-h and 12-h harmonic, see
Materials and Methods) were fitted to the respective means.
diurnal variation for the three test methods analogously to the evaluations used
for the measurement of fusion thresholds (Figure 2); none of these showed
significant diurnal variations (r < 0.6). To obtain an additional measure for
reliability similar to the two identical measurements of the fusion thresholds
(Figure 2), we performed two identical experiments using test method 3. The
SDs of two OTs measured at the same time of day were equally large as the
variation of means within 24 hours supporting the lack of a diurnally structured
variation.
In contrast to the fusion thresholds, the individual average OTs appeared to
be sex specific (females: 37.16 ms, males: 19.96 ms, Fig. 4). This difference is
highly significant (p ≤ 0.004, Mann-Whitney U-test).
DISCUSSION
Psychophysical experiments in the visual system have shown that threshold
sensitivities follow a clear diurnal rhythm, which is 180° out of phase with those
psychophysical functions which are mainly vigilance dependent (Roenneberg et
al., 1992). To contrast these sensitivity rhythms from antiphasic vigilance
24h changes in auditory temporal resolution
95
rhythms, we introduced the term of “sensory-dependent” diurnal time courses.
These sensory-dependent rhythms can only be seen when the quality of the
stimulus is easily and unambiguously recognized at its threshold. We measured
the sensitivity thresholds for light stimuli of different spectral composition in
several 24-hour experiments (Roenneberg et al., 1992) and found that both red
and blue stimuli were immediately recognized at threshold, while the intensity of
white and green stimuli had to be increased substantially above their detection
threshold before subjects could clearly recognize their actual quality. The former
had a clear sensory-dependent rhythms while the latter showed no significant
variation over the course of 24 hours. We concluded that this lack of rhythmicity
Fig. 3 – Diurnal time course for order thresholds (OT): Mean (circles) and standard deviation
(vertical lines) of all subjects in test 1 (bottom and lower left ordinate), test 2 (middle and right
ordinate), and test 3 (top and upper left ordinate). See also legend to Figure 2.
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Fig. 4 – Mean and standard deviations (vertical lines) for each subject of order thresholds (OT,
including all three test conditions) grouped by sex (bars representing male subjects are filled gray).
The mean for female subjects was 37.2 ms and the one for males 20.0 ms (dashed lines). These sexspecific differences are significant (p ≤ 0.004, Mann-Whitney U-test).
could be a consequence of two antiphasic diurnal rhythms, a sensory dependent
rhythm mainly modulating peripheral functions and a vigilance dependent one
mainly modulating central functions. If the detection of a stimulus is relatively
independent of central information processing (i.e., can clearly be recognized
already at its threshold) its diurnal time course will follow the sensory-dependent
type. If, however, the recognition of a psychophysical parameter is relatively
independent of peripheral functions (i.e., can only be computed well above its
detection threshold) or if its computation is independent of stimulus intensity, its
diurnal time course will follow the vigilance-dependent type. And finally, if both
peripheral and central processes are equally involved in the recognition, it may
not show any significant diurnal variation.
24h changes in auditory temporal resolution
97
This hypothesis has been substantiated by measuring the diurnal time courses
of several other psychophysical functions in different sensory modalities.
Auditory threshold sensitivity also follows a sensory-dependent rhythm when the
frequencies of the stimuli are in the optimal hearing range (M. Lotze and T.
Roenneberg, in preparation). Analogously to the ambiguity of green and white
light stimuli, subjects have great difficulties for several dB SPL around the
threshold to clearly detect acoustic stimuli outside the optimal hearing range
which results in a scattered but non-rhythmic distribution of thresholds over the
course of the day. Visual double pulse resolution (Treutwein and Rentschler,
1992) is known to be independent of stimulus intensity (providing it is well
above the threshold), and thus, its diurnal time course can be expected to be
vigilance-dependent. We found in 24-h experiments, that this is indeed the case
(M. Lotze, B. Treutwein, and T. Roenneberg, in preparation).
Another example of a sensory-dependent rhythm has been found for loudness
adaptation in the human auditory system (Pöppel, 1968b, 1968a). Unlike in all
the experiments described above and in the introduction, this experiment was
performed under true temporal long-term isolation, with extremely controlled
environmental conditions (including a constant background noise level) in the
famous “bunker” of Jürgen Aschoff and Rüdger Wever in the Max-PlanckInstitute of Erling Andechs (Aschoff and Wever, 1981). It is, thus, one of the
few psychophysical experiments measuring true circadian and not only a diurnal
(a single 24-h experiment under constant conditions) variations. A continuous
acoustic stimulus (in a “pleasant” hearing frequency) was presented to one ear
for 2 min. After it was turned off, subjects had to adjust the subjective loudness
of the adapting stimulus in the other ear. These experiments were repeated every
3 h over the course of 48 h. During the first 24 h, subjects were allowed to sleep
and were only woken for the measurements, while they were constantly awake
(like in the experiments described here) for the rest of the experiment. Under
both conditions, a clear circadian rhythm of auditory adaptation was found
with the least adaptation to the test stimulus around 3 a.m. It is interesting that
these circadian rhythms showed the same bimodality (i.e., a secondary maximum
at 3 p.m.) as the diurnal rhythm of fusion threshold measured in our
experiments.
In the hierarchy of temporal processing (Pöppel, 1997), the lowest threshold
(the fusion threshold) is known to be modality or receptor dependent. In
addition, lesions of left-hemisperic cortex regions impair the fusion threshold
only slightly (Lackner and Teuber, 1973). The next higher threshold (the order
threshold) is independent of the sensory modality (Hirsh and Sherrick, 1961) but
still depends on stimulus intensity (Berger-Gross and Bruder, 1984). We were
therefore interested, whether our observations also apply to these temporal
thresholds. The fusion threshold should follow a sensory-dependent diurnal
rhythm while the order threshold should not show a significant daily time
course, due to the fact that it requires central processing but also depends on the
stimulus intensity. The results of our experiments measuring these temporal
thresholds in the auditory system show that this prediction is true.
FTs show a significant diurnal time course, with performance maxima
(lowest FT) at night when vigilance is low (Figure 2). The time courses are best
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described with a composite sine curve containing two maxima. Similar bimodal
daily distributions are found when the sensitivity threshold is measured in the
optimal hearing range (M. Lotze and T. Roenneberg, in preparation). The lowest
auditory fusion performance (highest FT) around 12 a.m. coincides to best
vigilance dependent performance. The secondary performance troughs (note that
they are drawn as maxima in Figure 2) in all these experiments appear at the
time of lowest vigilance and may therefore represent its influence on detection.
Thus, the actual minimum of the rhythm’s sensory component may lie two or
three hours after midnight as it does in the case of visual thresholds, coinciding
with the vigilance trough.
In our experiments measuring the auditory order threshold, we applied three
different methods for the reasons given in the methods section. OTs depend on
the method of testing (Table I, bottom line), but did not show a significant
diurnal time course under any testing condition (Figure 3). This is supported by
the fact that identical measurements (using method 3) vary within one time unit
as much as they do over the 24-h time course. In contrast, two identical
measurements of FTs (Figure 2) showed only small variances within one time
unit and almost identical diurnal time courses.
In spite of the small number of subjects, our data indicate that OT-levels are,
in contrast to the FT-levels (Figure 1), sex-specific (Figure 4) as already
reported for other temporal tasks (Edwards, Squires, Buchwald et al., 1983;
Rammsayer and Lustenauer, 1989). Although such differences are still disputed
in the literature, they may contribute to understanding sex-specific differences in
brain anatomy and physiology (Goy and McEwen, 1980). The commisural
connections are surely involved in the temporal resolution of clicks presented to
both ears. Inter-hemispheric connections (Lacoste-Utamsing de and Holloway,
1982) as well as functional asymmetry (Kimura and Harshman, 1984) have been
shown to differ between women and men. Sex-specific differences in temporal
resolution tasks have also been reported in animals, namely a lateralization effect
to the left hemisphere for temporal resolution in male but not in female rats
(Fitch, Brown, O’Connor et al., 1993). The detection of OTs in humans appears
to depend mainly on left hemispheric cortical processes in both males and
females; they are only impaired in patients with left but not in those with right
hemispheric lesions (Steinbüchel v. et al., 1996). Higher OTs in female subjects,
as reported here, have also been found in a study involving both healthy control
subjects and patients with cerebral injuries (Wittmann, 1997).
OT-measurements have been applied clinically for the detection of speech
disturbances in aphasic patients which have been associated with an impairment
in the temporal resolution. The same was assumed for specific impairments of
language-learning in children (Tallal, 1980; Tallal, Stark and Mellits, 1985).
Training programs in non-verbal temporal discrimination by itself can improve
speech performance (Steinbüchel v., 1995; Steinbüchel v. et al., 1996) as well as
the combination of temporal training and speech therapy (Merzenich, Jenkins,
Johnson et al., 1996; Tallal, Miller, Bedi et al., 1996). The results described here
show that the time of day is not important for OT-measurements or for using
order thresholds in training programs, but will be of great importance in cases
where fusion thresholds are used for diagnosis and training.
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99
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Till Roenneberg, Institut für Medizinische Psychologie, Ludwig-Maximilians-Universität, Goethestrasse 31, 80336 München, Germany;
e-mail: [email protected]
(Received 9 March 1998; accepted 25 May 1998)