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CLINICAL NEUROSCIENCE - NEUROREPORT
Vol 13 No8
12 June 2002
Short-term hypobaric hypoxia enhances visual
contrast sensitivity
Krisztina Benedek, Szabolcs Kéri, Andor Grósz,
Zsolt Tótka, Erika Tóth and György Benedek
University of Szeged, Departments of Physiology,
Aero and Space Medicine, Neurology, and Psychiatry, Aeromedical Hospital,
Hungarian Defense Forces, H-6725, Semmelweis u. 6., Szeged, Hungary
Received 22 January 2002; Accepted 7 April 2002
The effect of hypoxia on early visual functions
remains a controversial arca of research. To explore this question, we
measured static and dynamic visual contrast sensitivity in 14 healthy
volunteers at a simulated altitude of 5500 m. In comparison with the baseline
condition (mean arterial oxygen satutation: 98.4%), contrast sensitivity significantly
increased after 5,10 and 15 min of hypoxic exposure {saturation: 82.9%,
77.0%, 74.3%, respectively). After 1O min, this enhancement was markedly
pronounced under dynamic conditions. Returning to the baseline altitude
(satutation: 97.7%), contrast sensitivity recovered, mostly at the lower
spatial trequencies. There was a significant negatíve relationship between
arterial oxygen satutation and contrast sensitivity values at low- and medium
spatial frequencies (0.5-4.8 cJdeg). These results suggest that early visual
processing may be enhanced during shoruterm hypoxic challenge.
INTRODUCTION
The availability of adequate amount of oxygen is a
crucial factor for the proper functioning of the nervous system. Cerebral
anoxia may cause marked neuropsychological impairment, affecting memory,
visuospatial functions and personality [1]. While most studies reveal
deficits in higher cognitive operations, including atlantion, executive
functions and memory [2-4], there is controversy regarding the question of early
visual functions such as contrast detection. Initfal reports showed increased
luminance thresholds in target detection tasks [5], but later studies hava
not observed impairment of visual contrast sensitivity [6,7]. It was
generally concluded that early visual functions are less altered by hypoxia,
while higher cognitive functions ara markedly disrupted [8]. In contrast to
this view, Flower et al. [9] proposed that prolonged reaction limes in visual
detection tasks ara due to the impairment of early visual information
processing.
To gain more insight into this area, we measured static and dynamic visual
contrast sensitivity at a simulated altitude of 5500 m. This altitude
provided a short-teret hypobaric hypoxia, which impaired attentional
processes in a previous experiment including a visual discrimination task
[10]. We used visual contrast sensitivity measurement because it is a
fundamental index of the integrity of early visual functions [11]. Contrast
is an essential parameter for perceiving a stimulus agarost its background,
for example as in the case of dark letters depicted on a white sheet of
paper.
In the present study we used computer-generated horizontal gratings with
different spatial and temporal frequencies to measure the minimal rnntrast
that is required for stimulvs detection (fig. 1.). This contrast threshold,
the reciprocal of which is called contrast sensitivity, was measured under
norma) and hypobaric hypoxic conditions. We hypothesised that hypoxia impairs
early visual functions, and therefore participants need higher contrast
thresholds under hypobaric hypoxic conditions to detect the gratings.
MATERIALS AND METHODS
Participants: Fourteen healthy male subjects with
norma) or corrected-to-norma) visual acuity participated in the study (mean
aga 32 years). All volunteers gave thait written informed consent. The
experimental protornl has been approved by the Eihical Committee of the
Albert SzentGyörgyi Medical Center, University of Szeged.
General arrasegement of the experiment: The experiment included the following
steps: (1) practice trial (dala not included in the analysis); (2)
measurement of baseline visual contrast sensitivity under norma) oxygen
pressure (first rnntrol); (3) measurement of visual rnntrast sensitivity
after 5, 10 and 15 min hypoxia in a hypobaric chamber (5500 m, 0.5 atm, 21
°C), in which it took 5 min to reach the simulated altitude; (4) measurement
of visual contrast sensitivity immediately after the normalisation of oxygen
pressure (sernnd wntrol). We therefore employed two normai (mntrol) und three
hypobaric hypoxic conditions. Arterial blood oxygen saturation, blood
pressure, heart rate. und electrocardiogram were monitored und recorded; a
physician was present in the chamber durrog the experiment. The contact between
the participant und the experimenter was maintained with an audiovisual
system.
V'isual contrast sensitivity: Binocular static und dynamic visual contrast
sensitivity was measured with a computerised test (Venus, NeuroScientific
Corporation, USA). Stimuli were horizontul luminance-contrast gratings with a
sinusoidal luminance profile (Fig. 1). Gratings rnnsisted of horizontul
stripes with periodically changing luminance (Lmax und Lmi;n). Contrast (C)
was defined by using the Michelson formula (C=(Lmax-Lmin)/(Lmax+Lmin)).
Spatial frequency was defined as the number of cycles/1° of visual angle
(c/deg). Visual contrast sensitivity was measured at nine spatial frequencies
(0.5,1.2,1.9, 2.9, 3.6, 4.8, 5.7, 7.2 und 14.3c/deg). In the static
condition, steady gratings were used. In the dynamic condition, gratings were
modulated at a temporal frequency (phase reversal) of 8Hz (Fig. 1). The
display, which was located outside the chamber, subtended a visual angle of
13 x 13°. The viewing distance was 1 m. The stimulus luminance was 9cd/m2.
The maximum contrast was 70.7%.
We used the following method for the measurement of contrast threshold.
First, the contrast was set at 15 dB above the mean normai value. The
contrast levei was decreased by 3 dB every 5 s for as long as the subject was
able to detect the stimulus (descending method). Contrast was then set at 15
dB below the threshold measured with the descending meíhod. For the ascending
method, the contrast was increased by 3 dB every 5 s up to the levei at which
the subject detected the stimulus. Contrast sensitivity was defined as the
reciprocal value of the contrast threshold. The sequence of the spatial
frequencies tested and the order of static and dynamic tests were
counterbalanced across subjects by the use of a pseudorandomly changing
schedule. In previous studies including dinical populations and normai
control subjecis, data obtained with this method were highly comparable to
visual contrast sensitivity values obtained with a more prolonged
two-alternative forced choice staircase method [12,13].
RESULTS
The participants tolerated the hypobaric hypoxic
condition well and reported no subjective visual problems. During hypoxia,
however, we observed a marked alteration in visual contrast sensitivity
functions. Iiaw data were log~ transformed and were entered into a 5
(condition) x 2 (temporal frequency) x 9 (spatial frequency) ANOVA. There
were main effects of condition (F(4,63) -12.30, p < 0.0001), temporal
frequency (F(1,63) = 5.05, p < 0.05), und spatial frequency
(F(8,504)=369.09, p < 0.0001). The condition x spatial frequency und the temporal
frequency x spatial frequency interactions were also significant (F(32,504)
-1.96, p < 0.002 und F(8,504) = 68.42, p < 0.0001, respectively). All
other interactions remained below the levei of statistical significance (p
> 0.1; Fig. 2).
To explore the origin of the condition x spatial
frequency interaction, three separate ANOVAs were conducted. First, the above
described three-way ANOVA was esed with four conditions (the first control
und the three hypoxic conditions). This ANOVA indicated main effects of group
(F(3,50) -14.82, p < 0.0001), temporal frequency (F(1,50) = 4.65, p <
0.05), und spatial frequency (F(8,400) = 292.69, p < 0.0001). While the
temporal frequency x spatial frequency interaction was significant (F(8,400)
= 49.44, p < 0.0001), the condition x spatial frequency interaction was
not (p = 0.98). When the two control conditions were rnmpared with the
three-way ANOVA, there was agaín a main effect of condition (F(1,26)=9.08, p
< 0.01), und the condition x spatial frequency interaction was aLso
significant (F(8,208) = 3.61, p < 0.001). Post hoc t-tests indicated that
the difference between the two control rnnditions was the largest at the
highest spatial frequencies (static: 7.2 c/deg: t(26) = -2.05, p = 0.05; 14.3
c/deg: t(26) = -2.06, p < 0.05; dynamic: 14.3 c/deg: t(26) = -3.50, p <
0.002, all other spatial frequencies p > 0.1; Fig. 2). When the hypoxic
conditions were compared with the second control, there was a main effect of
condition (F(3,50) = 3.91, p < 0.02). Again, the condition x spaűal
frequency interaction was significant (F(24,400) -2.31, p < 0.001); and
the rnndition x temporal frequency interaction also reached the levei of
statistical significance (F(3,50)=2.83, p < 0.05). When static and dynamic
contrast sensitivity values were averaged across spatial frequencies and were
compared with t-tests, the dynamic values exceeded the static values in only
one condition: after 10 min of hypoxic exposure (t(12)=-3.16, p < 0.01; in
all other conditions p > 0.1).
Spearman's rnrrelation coefficients (R) were calculated between the arterial
blood oxygen saturation and contrast sensitivity values. In both static and
dynamic conditions, there were significant negatíve correlations at low and
medium spatial frequencies (Table 1).
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Table 1. - Correlation between contrast and
arterial blood oxygen stuartion
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SF
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R static
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</>I>p</>P>static
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R dynamic
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</>I>p</>P>dynamic
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s.d. static
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s.d. dynamic
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0,5
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-0,61
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</> 0,0001
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-0,44
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</> 0,0002
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0,93
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0,42
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1,2
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-0,60
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</> 0,0001
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-0,61
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</> 0,0001
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0,83
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0,37
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1,9
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-0,58
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</> 0,0001
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-0,55
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</> 0,0001
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0,74
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0,41
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2,9
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-0,51
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</> 0,0001
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-0,59
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</> 0,0001
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0,68
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0,45
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3,6
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-0,41
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</> 0,0005
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-0,50
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</> 0,0001
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0,67
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0,48
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4,8
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-0,30
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</> 0,02
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-0,43
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</> 0,0005
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0,62
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0,50
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5,7
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-0,19
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> 0,1
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-0,10
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> 0,1
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0,59
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0,51
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7,2
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-0,10
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> 0,1
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-0,13
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> 0,1
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0,68
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0,61
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14,3
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-0,11
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> 0,1
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-0,14
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> 0,1
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0,89
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0,91
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SF, spatial frequency (c/deg), R, Spearman's
correlation coefficient, s.d.,standard deviations of the visual contrast sensitivity
data
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DISCUSSION
Agarost our initial hypothesis, we found
significantly increased contrast sensitivity values in hypobaric hypoxic
conditions achieved by a simulated altitude of 5500m. This finding is in contrast
to earlier reports [5-7], and suggests that early visual processes may be
enhanced during shortterm hypoxic challenge. At least three specific fartors
may contribute to this discrepancy: the degree of altitude, duration of
hypoxic challenge and stimulus luminance. Davis et al. [7] found reduced
visual acuity after 30 min at ~300m, but visual conírast sensitivity remained
unaltered durrog the whole testing procedure. Kobrick et aI. [6] used a very
high altitude (25 000 feet) in a gradually ascending manner and found no
contrast sensitivity alterations. In contrary, we observed a marked increase
after only 5 min of hypoxic exposure at 5500 m, which was sustained durrog
the whole 15 min experiment and promptly returned near to the baseline levei
after the normalization of oxygen pressure, with the exception of highest
spatial frequencies. These daca suggest that the degree of altitude and the
duration of hypoxic challenge may not explain the variability of results from
different studies. Another possibility is that different luminance levek
contributed to the heterogeneity of results, sínre higher luminance stimul
are less likely to be affected by hypoxia [6]. Nevertheless, increased
contrast sensitivity in short-term hypobaric hypoxic conditions has never
been documented before.
Although visual contrast sensitivity is considered as an index of early
visual processing predominantly mediated by retinai mechanisms [11], we
cannot exclude the possíbility that attentional fartors contributed to our
findings. However, attention is either impaired or unaltered in hypoxic
rnnditions [4], and this can hardly explain enhanced sensory processing. In a
previous visual discrimination tank performed in the same chamber at the same
altitude, subjecis showed significantly impaired attentional functions as
reflected by behavioural daca and event-related potentials [10].
The physiological effects of hypoxia on the visual system are poorly
understood despite its significance in dinical research and in applied
sciences such as aviation and space medicire. Electrophysiological
experiments investigating the cat retina revealed a marked resistance to
decreased oxygen availability. In general, photoreceptors are more sensüive
to hypoxia, because of their high oxygen rnnsumption and poor vascular
regulabon [14]. Schmeisser et al. [15] found thai physical exercise at
moderate altitudes (2200 m) decreased electroretinographic photopic flicker
responses, indicating a shift in retinai cone physiology Áltered oxygen
supply of the retina may have significantly contribution to various clinical
states such as photoreceptor dystrophies and diabefic retinopathy [16,17].
Harris et al. [18] found that hyperoxia improved visual contrast sensitivity
in patients with diabetic retinopathy. However, the effects of prolonged
hypoxia and short-term hypoxic challenge must be clearly distinguished. It
may be that mild and transient hypoxia increases reűnal sensitivity whereas
chronic prolonged síates lead to visual loss.
Another important issue is how hypoxia affects the parallel magnocellular and
parvocellular visual channels [19,20]. The present method allowed us to
measure contrast sensitivity at multiple spatial frequencies under both
static and dynamic conditions. This is an important point, because magnocellular
pathways are more sensitive for low spatial frequencies presented in a
dynamic condition, whereas parvocellular channels prefer static high spatial
frequency stimuli [19,20]. In general, the hypoxic challenge did not increase
visual contrast sensitivity in a strong spatial or temporal
frequency-speciftc manner. However, when the hypoxic conditions and the
sernnd rnntrol were compared, there was a more pronounced elevation for
dynamic values after 10 min hypoxic exposure. In addition, the level of
arterial oxygen saturation correlated inversely only with rnntrast
sensitivity values obtained at Jow and medium spatial frequencies. This
effect is not due to the restricted variance of contrast sensitivity data at
higher spatiaJ frequencies (Table 1). These findings raise the possibility
Ihat the magnocellular and parvocellular channels with distinguishable
spatial and temporaJ properties may be differentially affected by hypoxia.
CONCLUSIONS
Short-term hypobaric hypoxia significantly enhances
static and dynamic visual contrast sensitivity. The degree of enhancement at
low and medium spatial frequencies (0.5-4.8c/deg) inversely correlates with
the arterial blood oxygen saturation. The relationship of contrast
sensitivity enhancement wüh attentional alterations and visual magnocellular
and parvocellular functions under hypoxia warrant further investigation
because of its theoretical and clinical importance.
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