Journal of Vision (2009) 9(7):13, 1–12

http://journalofvision.org/9/7/13/

1

Spatial contrast sensitivity and grating acuityof barn owls
Wolf M. Harmening

Department of Zoology and Animal Physiology,
RWTH Aachen, Aachen, Germany

Petra Nikolay

Department of Zoology and Animal Physiology,
RWTH Aachen, Aachen, Germany

Julius Orlowski

Department of Zoology and Animal Physiology,
RWTH Aachen, Aachen, Germany

Hermann Wagner

Department of Zoology and Animal Physiology,
RWTH Aachen, Aachen, Germany

The eyes of barn owls (Tyto alba pratincola) display very little aberrations, and have thus excellent optical quality. In a seriesof behavioral experiments, we tested whether this presumably beneﬁcial feature is also reﬂected at a perceptual level in thisspecies. As fundamental indicators for visual performance, the spatial contrast sensitivity function (CSF) and grating acuity
were measured in two barn owls with psychophysical techniques. Stimulus luminance was 2.7 cd/m2. The CSF found here
renders the typical band-limited, inverted U-shaped function, with a low maximum contrast sensitivity of 8–19 at a spatial
frequency of 1 cyc/deg. Grating acuity was estimated from the CSF high frequency cut-off and yielded 3.0–3.7 cyc/deg. In asecond experiment, in which contrast was held constant and spatial frequency was varied, grating acuity was measured
directly (2.6–4.0 cyc/deg). These results put barn owls at the very low end of the visual acuity spectrum of birds, anddemonstrate that visual resolution and sensitivity cannot be predicted by optical considerations alone.
Keywords: spatial vision, contrast sensitivity, detection/discrimination, visual acuity, animal vision, barn owl
Citation: Harmening, W. M., Nikolay, P., Orlowski, J., & Wagner, H. (2009). Spatial contrast sensitivity and grating acuity ofbarn owls. Journal of Vision, 9(7):13, 1–12, http://journalofvision.org/9/7/13/, doi:10.1167/9.7.13.

Introduction
Barn owls are nocturnal predators which have evolved
specific sensory and morphological adaptations to a life
in dim light conditions. They are particularly renowned
for outstanding sound localization capabilities (Payne,
1971; Wagner, Brill, Kempter, & Carr, 2005) and ultrasilent flight (Bachmann et al., 2007; Graham, 1934).
Photoretinoscopy and, most recently, wavefront measurements of barn owl eyes demonstrated that they are
equipped with high-quality optics (Harmening, Vobig,
Walter, & Wagner, 2007b; Schaeffel & Wagner, 1996). In
particular, the amount of higher order aberrations in barn
owl eyes is only one third of what is found in human eyes
(Howland, 2002). This finding suggests paramount spatial
vision performance in barn owls, since retinal image
quality is shown to be extremely clear, theoreticallygranting a resolution equal to or higher than that of man(Harmening et al., 2007b). However, retinal ganglion celldensity was found to be comparably low, yielding alimiting Nyquist frequency that is by an order ofmagnitude lower than that calculated from human retinal
doi: 1 0. 11 67 / 9 . 7 . 13
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organization (Wathey & Pettigrew, 1989). Similar values
for a theoretical grating acuity can be deducted fromPERG measurements (Ghim & Hodos, 2006).
While higher processing stages of visual perception inbarn owls have been detailed in diverse approaches(Harmening, Göbbels, & Wagner, 2007a; Nieder &Wagner, 1999; Ohayon, Harmening, Wagner, & Rivlin,
2008; van der Willigen, Frost, & Wagner, 1998, 2002),
there is so far no account made to study the basics of spatial
vision on a behavioral level in these birds. We here present
for the first time a measure of both the contrast sensitivity
function (CSF) and grating acuity of barn owls in a set of
psychophysical experiments. If measured behaviorally, theCSF incorporates visual functions of both physical (i.e. thevisual transfer function of the eye) and physiological nature(i.e. visual processing in the nervous system) (Cornsweet,
1970; Graham, 1972; Westheimer, 1972). The CSF maytherefore be regarded as one of the fundamental functionaldescriptions of a visual system, and is a direct measure of
the perceptual high-level process of seeing. The CSF
together with a measure of grating acuity are finally used
to test whether the spatial vision thresholds of barn owls
match the excellent optics of their eyes.

Received February 24, 2009; published July 22, 2009ISSN 1534-7362 * ARVO

Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

Materials and methods
Subjects
Experimental animals were two male adult American barnowls (Tyto alba pratincola, subjects SL, PT), taken fromthe institute’s breeding stock. The birds were hand-raised
and tame. During the phase of experiments, body weight
was maintained at about 90% of their free feeding weight.
Water was given ad libitum, food (chick meat) was given
only in the experimental booth via a food dispenser or as areward directly after the experiment. Training and experiments took place on 5 days per week. The owls were fed intheir aviary when no experiment took place. Care andtreatment of the subjects was carried out in accordance withthe guidelines for animal experimentation as approved by
local authorities (Landespräsidium für Natur, Umwelt undVerbraucherschutz Nordrhein Westfalen, Recklinghausen,
Germany), and complied with the “NIH Guide for the use
and care of laboratory animals.”

Experimental setup and stimuli
All experiments were conducted in a sound and light
proof chamber (1.5 m  2 m  2.5 m), with no lightsource other than the stimulus display. The owls weresitting on a wooden perch in front of two response keys

2

that were symmetrically placed left and right to an
automated food dispenser. The head was unrestrained
and, upon the onset of a trial, oriented fronto-parallel
relative to the stimulus display. Viewing distance wasmeasured by observing the owl’s stereotypical pose under
infrared illumination, and equaled 85 cm, making one
pixel subtend 1.044 arcmin of visual angle (Figure 1).
Visual stimulus generation was controlled by custom
written software (ANSI-C with the Open-GL utility kit
GLUT), running on an Apple G5 workstation with a 8-bit
graphics board (NVidia Geforce 6800 GPU), and digitally
output on a 23W Apple Cinema Display (at its native
resolution, 1920  1200 pixel).
Two kinds of stimuli were used throughout this study.
One was a Gaussian filtered sinusoidal grating, often
called Gabor patch (hereafter referred to as Gabor). The
other stimulus was a sinusoidal grating, which was, except
for the Gaussian filter, identical to the Gabor (hereafterreferred to as Sinusoid). The stimuli could appear at two
discrete axes of orientation, i.e. the sinusoidal function
propagated either in 0- or 90- direction relative to thecoordinate system of the display (horizontal or verticalorientation, respectively, see Figure 1).
The standard deviation of the Gaussian of the Gabor washeld constant at 0.48. The phase of the sinusoidal function
was altered trial by-trial randomly in a 180- interval (not in
training sessions). The stimuli, 12.2 degree of visual angle indiameter, were shown centered on the screen when a trial
was initiated. The rest of the display was filled with a

Figure 1. A sketch of the experimental booth, showing the relevant parts of the experimental setup. The barn owl was sitting on a wooden
perch ﬁxed in front of an automated feeder, which delivered small pieces of meat upon correct responses (F). The two response keys
(L,R), corresponding to the two stimulus conﬁgurations, were in easy reach of the owl’s beak. Viewing distance (VD) was 85 cm. The
computer display was covered with a linear neutral density ﬁlter (ND) to reduce glare. This picture shows the situation when thehorizontal oriented Gabor patch was presented. A small IR-camera (C) monitored the owl’s gaze, which in case of a fronto-parallelorientation triggered trial progress. Note that except for the light originating from the display the room was completely dark underexperimental conditions.

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Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

uniform gray surface. The background was black when the
Sinusoid was presented. The whole screen was covered witha large sheet of linear neutral density filter (Lee Filters, UK)that lowered overall luminance by approximately one log
unit, producing a mean luminance of 2.74 cd/m2, equallydistributed within the stimulus area. The filter was removed
for grating acuity experiments with one animal only (meanluminance: 30 cd/m2). Stimulus contrast was controlled bymodification of the amplitude of the sinusoidal function andwas measured at viewing distance in a pre-experimental
calibration sequence with a luminance meter (LS-100, Konica
Minolta). Our display system was able to reliably produce
stimulus contrasts ranging from 0.99 to 0.01, whereby aliasing
artifacts could be excluded due to psychophysical tests with ahuman observer. Contrast is defined throughout this study
according to the Michelson-formula (1):CM ¼

lummax j lummin:lummax þ lummin

ð1ÞThe choice of spatial frequencies used in the training
sessions and experiments followed observations from pilot
testing and earlier studies with the same subjects andsetup (Harmening et al., 2007a).

Psychophysical procedures
A small, flashing fixation target was shown in the center ofthe display between trials to attract the owls’ gaze and tosupport correct orientation. When the subject oriented its
gaze toward the screen, a trial was initiated and the stimulus
was shown. After stimulus onset the owls had to peck one of
the two response keys, corresponding to either a horizontal(right key) or vertical (left key) orientation of the grating.
The right-left/horizontal-vertical association was used forboth animals. Horizontal or vertical gratings were presented
in a pseudo-random order, i.e. no more than three repetitionsof one of the two alternatives were presented consecutively.
The owls were rewarded after every correct response, false
responses were not punished. The time course was selfpaced to allow an exact observation of the stimulus.
Whenever the owls made large head movements and stopped
fixating the display, a trial was aborted. Possible accommodation during experiments was not monitored.
Both owls were extensively trained to discriminate thetwo different orientations correctly before experiments
began. Because the animals were involved in psychophysical two-alternative forced choice (2-AFC) tasks before(Harmening et al., 2007a), the orientation discrimination
task could be progressively introduced as transfer tests intraining sessions. During this training phase the stimulus
contrast, its spatial frequency, and the phase position of
the sinusoid was held constant (contrast: 0.99, spatial
frequency: 0.61 cyc/deg, phase: 90-). When owls reachedsignificant performance in the task (i.e. performance washigher than 85% correct), the experimental phase began.

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Prior to contrast sensitivity experiments, several control
experiments were conducted (684 trials). First, thepseudo-random design of the trial sequence was altered toallow up to 7 repetitions of one alternative consecutively.
This control intended to rule out strategy learning in thesubjects, making them, at low stimulus intensities,
guessing better than chance level. Second, to exclude
learning of stimulus feature other than orientation, stimuli
with (a) random phase (0–180-) and (b) random
spatial frequencies drawn from a predefined interval(1.5–0.5 cyc/deg) were rendered at maximum contrast. In
all control sessions, the owls responded more than 85% of
the time correctly.
Typically, a single experimental session consisted ofabout 30 to 50 trials. Each session was conducted at asingle spatial frequency, or, in grating acuity experiments,
at a single contrast level. A simple staircase procedure
was employed: stimulus intensity progression within asession followed an up-down transformed rule. That is,
stimulus intensity (i.e. contrast in the CSF experiments,and spatial frequency of the grating in grating acuity
experiments) was decreased after two consecutive correct
responses and was increased after every false response. In
this way, converging to stimulus intensities at which theanimal responded 70.7% of the time correctly, the choiceof stimulus intensities presented to the animal lay near thethreshold. To prevent fatigue and frustration of the owl at
low stimulus intensities, bonus trials at high intensities
were given from time to time. Spatial frequencies used in
CSF experiments ranged from 0.4 to 2.4 cyc/deg, and,thus, covered about 2.6 octaves. To avoid systematic
impact of learning processes, spatial frequencies across
CSF experiments were applied in a non-systematic order.
For further analysis, the results of two consecutive
experimental sessions at each spatial frequency werecombined to build the basis of psychophysical raw data.
This was done by re-calculating the performance level at
each stimulus intensity from the pooled data of both runs.
The psychophysical raw data was further combined across
two or more experimental days (see Figure 2 for an
example). Due to the adaptive staircase, this procedure
increased the number of trials presented below thetargeted threshold, and, thus, increased the validity ofsubsequent curve fitting. Furthermore, the combination
balanced out inconsistencies in animal performance thatsometimes occurred on different testing days. Note that it
did not necessarily produce an average threshold of theindividual runs.

Data analysis
For all spatial frequencies, the combined behavioral
performance, i.e. the percentage of correct responses, wasplotted as a function of stimulus intensity. With aJournal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

4

Figure 2. The method of data pooling used throughout this study. In this example, results from owl PT in the contrast sensitivity experiment(@ 1.41 cyc/deg) are shown. In (a) individual staircase runs from four experimental days (I–IV) are plotted. Dashed lines represent highintensity bonus trials. The two horizontal lines correspond to the threshold level calculated from the combined data (compare (c), 74.3%
correct), and the theoretical convergence level of the 2down-1up method (70.7% correct), respectively. Note that many trials wereconducted in close proximity of the threshold. In (b) results from each day (I–IV) were combined and expressed as psychometricfunctions. The ratio of correct responses is denoted on the y-axis. Contrast threshold and, inversely, contrast sensitivity (CS) were
calculated from ﬁtting a logistic psychometric function to the data, and were deﬁned at the inﬂection point of that function. The small
horizontal bar is the 95% conﬁdence interval at threshold level. N is total trial number. In (c) the results of the four days are combined byre-calculating the performance at each contrast level for the pooled data from (b). The distribution of number of trials across stimulus
intensities is given in the bar plot at the bottom.

parametric bootstrap method described by Wichmann and
Hill (2001a) used in the Matlab function pﬁt, a logistic
function <(x) was ﬁtted to the data points, generating acomplete psychometric function (2).
<ðxÞ ¼ + þ ð1j + j 1Þ 

1
!jx

1þe "

;

ð2Þ

where <(x) is behavioral performance at stimulus intensity x, ! and " are the fit parameters. Threshold was

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defined as the stimulus intensity on the psychometricfunction half-way between lower (+) and upper (1)asymptote, at the inflection point of that function. + wasnumerically fixed at 0.5, reflecting the 2-AFC design ofthe experiment. 1 was corrected to account for lapses(false responses) the owl frequently showed at highstimulus intensities (lapse-rate interval {0,0.2}). The
parametric bootstrap method (re-sampling n = 1000) was
also used to obtain an estimate of the 95% confidence
level of each individual threshold (Wichmann & Hill,Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

stimulus. This value corresponds to a Michelson contrast
of 0.051. A similar value could be found with the Sinusoid(18.7, CI: 17.0–20.8). Sensitivity values decreased monotonically with both higher and lower SFs. At the highest
SF tested with the Gabor (2.2 cyc/deg) sensitivity dropped
to 2.2 (CI: 2.0–3.0), and to 2.6 (CI: 2.3–3.7) at 2.4 cyc/deg
with the Sinusoid. The lowest SF tested with SL (0.4 and0.5 cyc/deg, respectively), yielded sensitivity values of
2.7 (CI: 2.2–3.3) for the Gabor, and 4.2 (CI: 3.8–4.7) for
the Sinusoid. Generally, the results from the two
stimulus configurations in SL were very similar. In owl
PT, highest sensitivity appeared at the same SF as in SL,
but with decreased magnitude (CS: 8.1, CI: 7.3–9.2),
corresponding to a Michelson contrast of 0.124. The
same observation, a reduction of absolute sensitivity toabout one half of the values found in SL, holds for all
spatial frequencies tested. The terminal SFs (0.5 and2.0 cyc/deg, respectively) yielded sensitivity values of
2.6 (CI: 2.4–2.7) and 3.7 (CI: 3.3–4.4).

2001b). Contrast sensitivity was expressed as the inverseof the Michelson contrast at threshold level.
A double exponential function (3) was fitted to thesensitivity normalized data by a method of least squares.
This four-parameter function was found to provide a good
fit to the CSF of several species (Uhlrich, Essock, &Lehmkuhle, 1981).
Sð3Þ ¼ 100ðK1 ej2:!3 j K2 ej2:"3 Þ;ð3Þwhere S(3) is contrast sensitivity at spatial frequency H.
Grating acuity was derived computationally from an
extrapolation of the CSF beyond the high frequencies
tested (max{S(3) = 1}). Additionally, grating acuity wasmeasured directly in a way similar to the method
described above: at maximum contrast (cM = 0.99) spatial
frequency was altered according to the transformed updown rule. A psychometrical function was then fitted tothe behavioral discrimination performance at the different
levels of spatial frequency. The grating acuity threshold
was defined as the spatial frequency at the inflection pointof the corresponding psychometric function. Confidence
intervals were calculated as stated above.

Grating acuity
Grating acuity was measured at the highest contrast
possible to be displayed (cM = 0.99), and was defined as
the SF of the sinusoidal function at which discrimination
performance was at threshold level. In addition todiscrimination, a detection paradigm was applied inexperiments with the Sinusoid. Here, gratings were
presented in horizontal configuration only, while thenull-stimulus was a uniform gray surface with identicalmean luminance (depicted as a small inset in Figure 3a).
Measured with the Gabor, owl SL displayed a grating
acuity of 3.95 cyc/deg (CI: 3.82–4.12 cyc/deg). In
detection experiments grating acuity was 3.43 cyc/deg(CI: 3.22–3.78 cyc/deg). Discrimination performance with
the Sinusoid yielded a grating acuity of 3.23 cyc/deg

Results
Contrast sensitivity
Contrast sensitivity was expressed as the inverse of thestimulus contrast at which discrimination performance
was at threshold level (compare Table 1 and Figure 4). A
maximum contrast sensitivity (CS) of 19.6 (confidence
interval (CI): 17.9–23.2) was found in subject SL at a
spatial frequency (SF) of 1 cyc/deg with the Gabor

SL(G)

5

SL(S)

PT(S)

SF

CS

CI

n

p.thr

SF

CS

CI

n

p.thr

SF

CS

CI

n

p.thr

2.2
2.0
1.5
1.2
1.0
0.9
0.8
0.6
0.5
0.4

2.2
10.1
14.9
16.0
19.6
15.6
8.7
5.3
3.5
2.7

2.0–3.0
9.3–11.4
13.0–16.7
15.1–17.2
17.9–23.2
14.3–17.2
7.7–10.0
4.3–6.8
3.1–4.5
2.2–3.3

146
340
188
290
263
176
198
432
171
201

.702
.729
.726
.693
.721
.750
.737
.702
.718
.711

2.4
2.0
1.5
1.0
0.8
0.5

2.6
7.0
10.4
18.7
8.7
4.2

2.3–3.7
6.3–7.9
9.6–12.7
17.0–20.8
8.0–9.5
3.8–4.7

84
139
81
222
363
282

.701
.732
.737
.732
.726
.730

2.0
1.7
1.4
1.0
0.8
0.6
0.5

3.7
5.0
7.7
8.1
5.4
4.5
2.6

3.3–4.4
4.6–5.6
7.1–8.5
7.3–9.2
5.1–6.0
4.3–4.9
2.4–2.7

295
170
240
290
236
185
389

.671
.730
.742
.712
.740
.750
.744

Table 1. Results from contrast sensitivity experiments across subjects (PT, SL) and conditions (G: Gabor, S: Sinusoid). Contrast sensitivity(CS) values at all spatial frequencies (SF [cyc/deg]) are given, together with the 95% conﬁdence interval borders (CI), the number oftrials (n), and the performance level at which threshold was deﬁned (p.thr).

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Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

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Figure 3. Results from grating acuity (GA) experiments. (a) Top row: measurements in owl SL, bottom row: owl PT. The ratio of correct
responses is plotted against spatial frequency (SF). The circles denote discrimination performance at a given SF. The solid line is thelogistic ﬁt to the data, the small horizontal bar is the 95% conﬁdence interval (CI) at threshold. The majority of trials were conductedaround threshold level (see bar plot at the bottom of each panel, denoting trial numbers (n) per stimulus intensity). The small inset on theleft part of each panel denotes experimental condition: Gabor and Sinusoid stimuli, detection and discrimination tasks. (b) Comparison ofindividual runs across animals and conditions. Circles are results from owl SL, diamond markers denote results from owl PT. The verticalbars are the CIs, the smaller horizontal bar is the threshold from (a). As a reference, the dotted lines represent earlier results from patternelectroretinogram (PERG) measurements (Ghim & Hodos, 2006), and ganglion cell (GC) count (Wathey & Pettigrew, 1989).

(CI: 2.90–3.44 cyc/deg). With this animal only, we
performed grating acuity experiments in 1476 trials at aten-fold higher mean stimulus luminance (30 cd/m2), andthe threshold was marginally lower (4.07 cyc/deg,
CI: 3.95–4.18 cyc/deg). Owl PT performed grating acuity
experiments with the Sinusoid only. In detection experiments grating acuity was the lowest reported, and yielded
1.64 cyc/deg (CI: 1.41–1.87 cyc/deg). Grating acuity wasmeasured twice in the discrimination task, as a test and retest control. In the first measurement, grating acuity was
2.03 cyc/deg (CI: 1.88–2.33 cyc/deg). In the re-test,
grating acuity was 2.58 cyc/deg (CI: 2.44–2.76). The
results of the individual experimental runs were all higher
in later measurements. Thresholds were (in chronologicalorder): 1.51, 1.06, 1.45, 1.56, 2.25 cyc/deg in detection
experiments, and 1.65, 1.56, 1.89, 2.21, 2.29, 2.61, 2.66,
2.73 cyc/deg in discrimination experiments. See Figure 3b
for results of all individual staircase runs and also for acomparison of grating acuity results across animals andconditions with reference to earlier electrophysiologicaland anatomical estimates (result from higher luminancelevel not shown in figure).

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Contrast sensitivity function
Contrast sensitivity values derived from the combined
experimental sessions were plotted against spatial frequency on a double logarithmic scale (see Figure 4).
Sensitivity values increased strictly monotonic from low
spatial frequencies up to intermediate spatial frequencies,
where sensitivity was maximal at 19.6, 18.7, and 8.1 at
1.01 cyc/deg for owl SL(Gabor), owl SL(Sinusoid), andowl PT(Sinusoid), respectively. Consistently, going further to higher spatial frequencies, sensitivity decreased
strictly monotonic in both animals.
According to Equation (3), our best fit for the pooleddata of both owls for both the Gabor and the Sinusoid
was found for the following parameters: K1 = 1.4989,
K2 = 1.5230, ! = 0.2630, " = 0.2691 (normalization
factor: 19.61). Peak sensitivity derived from this function
was 12.58 at a spatial frequency of 1.01 cyc/deg. The
width of the CSF was measured in octaves as the
distance between the spatial frequency on either sideof the peak frequency at which sensitivity declined bya factor of two. Thus, width at half amplitude wasJournal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

7eyes predict resolution capabilities that are at least anorder of magnitude better than the behavioral acuity
reported here.

Methodological considerations

Figure 4. The behavioral contrast sensitivity function of barn owls.
Contrast sensitivity was deﬁned as the inverse of contrast
threshold and was plotted against spatial frequency. The different
markers represent the two animals and conditions (legend). The
vertical bars are the 95% conﬁdence intervals calculated from the
combined psychometric functions. Small dots are results fromindividual runs. Sensitivity values were ﬁtted to a double
exponential function, plotted as dashed lines for the different
conditions, and as solid line for pooled data. Results from grating
acuity experiments are plotted for reference as well (bottom right).

1.88 octaves (0.55–2.02 cyc/deg). The high frequency
cutoff, max{S(3) = 1}, was 3.51 cyc/deg. The according
values were calculated for individual results, and areshown as their corresponding function in Figure 4.

Discussion
The data presented here are the first measure of the
behavioral spatial contrast sensitivity function and grating
acuity in the visual system of barn owls. A mean
maximum contrast sensitivity of around 12 was found at
a spatial frequency of 1 cyc/deg. Sensitivity declined
rapidly for spatial frequencies lower than 0.8 cyc/deg andhigher than 2 cyc/deg. Width at half amplitude was rather
narrow, with a mean of 1.8 octaves. Grating acuity asderived from the high-frequency cut-off of the CSF was
between 3.0 and 3.7 cyc/deg. Furthermore, grating acuity
was reported independently in a second behavioral
experiment. Here, grating acuity values between 2.6 and
4.0 cyc/deg were found. These results constitute a
pronounced optics-acuity disagreement in these animals,
because calculations based solely on the optics of their

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A detailed ROC analysis combining data from bothanimals across experimental conditions revealed no significant or systematic response bias towards one of thetwo alternative stimulus orientations. Similar to our
results, a lack of an orientation anisotropy for the principal
orientations (horizontal/vertical) was reported from CSF
measurements in human and cat subjects (Bisti & Maffei,
1974; Campbell, Kulikowski, & Levinson, 1966).
Based on the results of the control experiments, weconclude that the owls were able to incorporate a conceptof the orientation discrimination task. In transfer trials,
with gratings of spatial frequencies that were never usedin the training sessions before, the owls showed similar
performance as in the training sessions. This was also thecase when the grating was presented with random phase
configuration. Moreover, the responses to the stimulus
showed robustness against a change in inter-trial alternative choice to a quite large extent. While in training
trials no more than three repetitions of one alternative
occurred consecutively, this was changed to a maximumof 7 possible consecutive repetitions in the control
sessions. Again, performance did not drop significantly,
although this change might have increased fatigue andfrustration in the owl. We conclude from this, that theapplied psychophysical method and stimuli produced astable behavioral response in the animals.
In one animal (PT), learning processes might have had
influences on grating acuity estimates. That is, during thecourse of experiments, thresholds generally improved. A
look at the corresponding psychometric functions of a test
and re-test (Figure 3) reveals that baseline performance athigh intensities differ to a large extent (85% correct, and
99% correct, respectively). As a consequence, grating acuityin this animal is reported as the performance displayed inthe (chronologically) last experiment (2.58 cyc/deg).

Signiﬁcance of the results
For validation, our results can be compared to at least
two studies, in which contrast sensitivity and grating
acuity of barn owls was measured and computed electrophysiologically and anatomically, respectively (Figure 5).
In the electrophysiological study, the authors measured
contrast sensitivity in 4 barn owls with the patternelectroretinogram (Ghim & Hodos, 2006). Combined
peak sensitivity of about 6 was found at a spatial
frequency of 1.1 cyc/deg (Figure 5). In this study, grating
acuity (6.98 cyc/deg) was computed based on extrapolation

Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

8

the CSF, and, therefore, grating acuity estimates to alarge extent (Bisti & Maffei, 1974; Blake, Cool, &Crawford, 1974; De Valois & Morgan, 1974; Jacobs,
1977; Patel, 1966).
In an anatomical study, the retinal ganglion cell density
was used as the basis for a grating acuity estimation. A
maximum ganglion cell density of 11000–12500/mm2 wasreported at the area centralis, and, thus, a grating acuity of
7.9–8.4 cyc/deg was calculated by application of the
Shannon sampling theorem and an assumptive retinal
magnification factor of 0.15 mm/deg (Wathey & Pettigrew,1989). While the geometry of barn owl eyes is describedin detail (Schaeffel & Wagner, 1996), it remains unclear
how many of the ganglion cells in area centralis are
involved in spatial acuity tasks. Moreover, considering the
topography of ganglion cell density in the retina of barnowls, displaying a horizontal streak of lower cell density(5000–8000/mm2), behavioral acuity values lower than
the theorized 8 cyc/deg become reasonable (Wathey &Pettigrew, 1989).

Figure 5. Comparative view on contrast sensitivity and grating
acuity of barn owls and other animals. Open markers and blacksolid line are the contrast sensitivity values and CSF found in thepresent study. Filled markers and gray solid line are a re-plot of
the barn owl CSF found by Ghim and Hodos (2006) with thepattern electroretinogram (PERG). Mean grating acuity (GA)found in our study is shown as open star, a gray star marks thegrating acuity estimate based on ganglion-cell count by Wathey
and Pettigrew (1989). The inset at the top right compares CSFs
across several species. These plots are re-drawings of either
mean or representative results. References are: human (Berkley,1976), macaque (De Valois, Morgan, & Snodderly, 1974), cat(Bisti & Maffei, 1974), goldﬁsh (Northmore & Dvorak, 1979),
kestrel (Hirsch, 1982), eagle (Reymond & Wolfe, 1981), andpigeon (Hodos et al., 2002).

of the CSF beyond the measured high spatial frequencies,
similar as in the present study. While the spatial frequency
at which sensitivity peaks is in good accordance with our
results (1 cyc/deg), data with respect to maximum
sensitivity values, bandwidth, and high frequency cut-off
are at variance with the present results. This might bedue to the different methodological approach: the PERG
method is known to produce about 40% differences inpeak sensitivity when compared to behavioral data in thesame subject (Hodos, Ghim, Potocki, Fields, & Storm,
2002; Peachey & Seiple, 1987). Bandwidth and grating
acuity differences might be due to different luminancevalues used for visual stimulation. In the PERG study,
mean luminance of the display was 94 cd/m2. Our
experiments were conducted at intermediate light levels(2.7 cd/m2), a more than 30 fold reduction of mean
luminance. In human, primate, and cat subjects it has
been shown that a reduction of stimulus luminance affects

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Inter-species comparison
How do the results presented here compare to data fromother birds and animals? A rather qualitative answer isgiven with the inset of Figure 5. Common with all birds
that have been tested so far, barn owls display a relatively
low maximum sensitivity (below 20). Bird maximum
contrast sensitivity has so far never exceeded 30, or
expressed as Michelson contrast, 0.03. Given that birds
are generally regarded as highly reliant on visual
information, this finding is surprising and still unsolved
as to which mechanisms are responsible for this relatively
low sensitivity (Hodos, Ghim, Miller, Sternheim, &Currie, 1997). The barn owl behavioral CSF is narrower
than any other CSF, which might be simply explained by
the illumination conditions used in our experiments. On
the other hand, it might reflect the presence of only
few, narrowly tuned spatial frequency channels (Irvin,
Casagrande, & Norton, 1993). A comparison with PERG
results in which bandwidth is clearly increased (Ghim &Hodos, 2006) would then dictate the origin of this effect tobe strictly post-retinal. While small bandwidth and low
contrast sensitivity are all common among bird CSFs, thelocation of the CSF on the spatial frequency axis differ
among species. This is easily explained by the individual
maximum acuity the birds exhibit. While the eagle andkestrel, both equipped with high resolution capabilities(70–140 cyc/deg), have CSFs with maximum sensitivity at
a spatial frequency of around 10 cyc/deg, the pigeon andbarn owl’s maximum sensitivities are shifted towards lower
spatial frequencies, lying somewhere around 1 cyc/deg.
Consistently, these two species have maximum resolutions (pigeon: 6 cyc/deg, barn owl: 3.3 cyc/deg) thatare essentially lower than those of the two raptorial
species.

Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagner

Interestingly, especially in the light of the excellent
optical quality of barn owl eyes, the behavioral resultsfrom grating acuity experiments reported in our study(2.6–4.0 cyc/deg) put barn owls at the very low end of theacuity spectrum of birds that were tested at similar
luminances. Other owls, like little owls (6 cyc/deg)(Porciatti, Fontanesi, & Bagnoli, 1989), great horned owls
(6–7.5 cyc/deg) (Fite, 1973), and tawny owls (8 cyc/deg)(Martin & Gordon, 1974), have slightly higher maximum
resolutions. Generally, compared to other raptorial birds,
owls lie on the lower end of the acuity spectrum, possibly
because their hunting success is less reliant upon vision
than this is the case for diurnal raptors. Known behavioral
acuity values in raptors span from extraordinary highSpecies name9values in wedge tailed eagles (140 cyc/deg) (Reymond, 1985;
Schlaer, 1972), to manlike values of around 70 cyc/deg inAustralian brown falcons (73 cyc/deg) (Reymond, 1987)
or American kestrels (about 50 cyc/deg) (Hirsch, 1982).
Superb acuities of 160 cyc/deg in an American kestrel(Fox, Lehmkuhle, & Westendorf, 1976) have beenquestioned due to an about 3 fold lower anatomical
resolution (46 cyc/deg) (Dvorak, Mark, & Reymond,1983), and were re-tested in an electrophysiological study(39.7–71.4 cyc/deg) (Gaffney & Hodos, 2003). Grating
acuity of some other non-raptorial birds have beenmeasured, either electrophysiologically or behaviorally,
and the results place them somewhere between owls andeagles on the acuity scale. Among those are for example

Acuity [cyc/deg]@luminance[cd/m2]

Barn owl (Tyto alba pratincola)
Little owl (Athene noctua)
European robin (Erithacus rubeculus)
Great Horned Owl (Bubo virgianus)
Reed bunting (Emberiza schoeniclus)
Domestic chick (Gallus gallus domesticus)

2.6–4.0/4.1
6a
6/6
6–7.5
2.17/7.8
4.2–6.4/7.7–8.6

2.7/30200
1.53/19.1
80
1.53/19.1
3.5/65

Yellowhammer (Emberiza citrinella)
Tawny owl (Strix aluco)
Pigeon (Columba livia)
Blue Jay (Cyanocitta cristata)Peafowl (Pavo crystatus)
Skylark (Aulada arvensis)
Fieldfare (Turdus pilaris)
Blackbird (Turdus merula)
Chafﬁnch (Fringilla coelebs)
Sacred kingﬁsher (Halcyon sancta)
Rook (Corvus frugilegus)
Jackdaw (Corvus monedula)
Magpie (Pica pica)
Laughing kookaburra (Dalceo gigas)
American kestrel (Falco sparverius)
American kestrel (Falco sparverius)

2.17/9.7
8.8/12/8–11.1
3/6/12/18
15–19b
20.6b
22.5/11.4
22.5/15.9
22.5/22.5
22.5/22.5
26b
29.5/29.5
13.0–23.7/29.5–33.3
23.7–29.5/29.5–33.3
41b54/100/160
46b/39.7–71.4a

1.53/19.1
5/50.5/160
0.85/3.2/32/317––
1.53/19.1
1.53/19.1
1.53/19.1
1.53/19.1–
9.5/609.5/609.5/60–3.5/35/350–/93

Australian brown falcon (Falco berigora)
African serpent eagle (Dryotriorchus spectabilis)
Wedge tailed eagle (Aquila audax)

52/73
120c
30–40d/58/138

2/2000–2/20/2000

Goldﬁsh (Carassius auratus)
Galago (Galago crassicaudatus)
Cat (Felis catus)
Macaque (Macaca nemestrina/fascicularis)
Human (Homo sapiens)

1.4–2.2
2.6–4.3
5.0d
31/46
35/50

5
22
2
1.7/171.7/17

Reference
Harmening, present study
Porciatti et al. (1989)
Donner (1951)
Fite (1973)
Donner (1951)
DeMello, Foster, and Temple (1992),
Schmid and Wildsoet (1998)
Donner (1951)
Martin and Gordon (1974)
Hodos et al. (1976)
Fite and Rosenfield-Wessels (1975)
Hart (2002)
Donner (1951)
Donner (1951)
Donner (1951)
Donner (1951)
Moroney and Pettigrew (1987)
Dabrowska (1975)
Dabrowska (1975)
Dabrowska (1975)
Moroney and Pettigrew (1987)
Fox et al. (1976)
Dvorak et al. (1983), Gaffney andHodos (2003)
Reymond (1987)
Schlaer (1972)
Reymond (1985), Reymond andWolfe (1981)
Northmore and Dvorak (1979)
Langston et al. (1986)
Bisti and Maffei (1974)
De Valois and Morgan (1974)
De Valois and Morgan (1974)

Table 2. An overview of visual acuity thresholds across bird species, ordered by the maximum acuity exhibited. Where possible, resultsthat were obtained at similar luminances as used in our experiments are shown. A few non-avian species are given for comparison.
Note: Grating acuity estimated by: aelectroretinogram, bganglion cell count, coptics, dCSF.

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Journal of Vision (2009) 9(7):13, 1–12

Harmening, Nikolay, Orlowski, & Wagnersome passerine birds (2.2–22.5 cyc/deg) (Donner, 1951),
domestic chicks (7.7–8.6 cyc/deg) (Schmid & Wildsoet,1998), Blue Jays (15–19 cyc/deg) (Fite & RosenfieldWessels, 1975), pigeons (18 cyc/deg) (Hodos, Leibowitz,& Bonbright, 1976), rooks (29.5 cyc/deg), and magpies(29.5–33 cyc/deg) (Dabrowska, 1975) (compare Table 2
for an elaborated list of visual acuity in birds).

The optics-acuity disagreement
The grating acuity of the two barn owls tested here is ofa magnitude comparable to results found in cats (5.0 cyc/deg)(Bisti & Maffei, 1974) and galagos (2.6–4.3 cyc/deg)(Langston, Casagrande, & Fox, 1986), a prosimian
primate. This observation across animal species of suchdivergent phylogenetic origins supports the speculationthat their common nocturnal lifestyle is the most important ecological factor setting the limits of spatial vision inthese animals (Warrant, 2004). What remains rather
surprising in this respect is why barn owls display suchremarkably high-quality optics while visual acuity is poor.
In fact, our results suggest that spatial vision in barn owls
is among the worst ever recorded in a bird, and opticalquality is among the best ever measured in any vertebrateeye (Harmening et al., 2007b). The former finding, albeit
known from other owl species, contrasts the commonly
accepted superb visual capabilities in birds of prey.
Put together, both findings constitute a remarkable opticsacuity disagreement in the barn owl visual system. A
similar discrepancy was observed in a wavefront study ofcat eyes (Huxlin, Yoon, Nagy, Porter, & Williams, 2004).
In contrast, it is well established that the anatomical andbehavioral resolution of humans and other high-acuity
animals like for example the wedge-tailed eagle match theoptical transfer characteristics of their eyes very well(Campbell & Green, 1965; Reymond, 1985). A match in
optics and acuity may be a reasonable design feature,
because an undersampling of the retinal image through acoarser sensory array would impose visible moir’epatterns onto the perceived image (Barlow, 1981;
Williams, 1985). Also, other interference effects comeinto play which may ultimately degrade spatial vision(Coletta, Williams, & Tiana, 1990). Whether barn owls
perceive interference patterns due to retinal undersampling is unclear. However, if this would actually be thecase, their resolution capacity could have shifted beyond
the limits set by the photoreceptor lattice, which would
be then visible in our grating acuity experiments (Thibos,
Walsh, & Cheney, 1987). This was not observed. We
suggest that the presence of low higher-order aberrations(HOA) is a beneficial feature also for low-acuity animals
who are active at mesopic or scotopic luminanceconditions, because HOA are known to produce visual
deteriorations such like glare, halos, ghost images, andgeneral blurring, which are probably disadvantageous
regardless of the visual resolution its bearer exhibits. It

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10

would be interesting to study aberration properties in alarger set of species, to maybe discover that low HOA isa common optical design feature across animals thatshare relatively low visual acuity and a crepuscular/
nocturnal lifestyle.

Acknowledgments
We thank an anonymous reviewer for elaborated andconstructive comments on an earlier version of the manuscript.
Commercial relationships: none.
Corresponding author: Dr. Wolf M. Harmening.
Email: wolf)bio2.rwth-aachen.de.
Address: Department of Zoology and Animal Physiology,
RWTH Aachen, Mies-van-der-Rohe-Str. 15, 52056 Aachen,
Germany.

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