Sato (2012) The effect of water immersion on short latency somatosensory evoked potensials in hum

R E S E A R C H A R T I C L EOpen Access
The effect of water immersion on short-latency
somatosensory evoked potentials in human
Daisuke Sato1,2*, Koya Yamashiro1,2, Hideaki Onishi1,3, Yoshimitsu Shimoyama2, Takuya Yoshida1,2and
Atsuo Maruyama1,2
Abstract
Background: Water immersion therapy is used to treat a variety of cardiovascular, respiratory, and orthopedic
conditions. It can also benefit some neurological patients, although little is known about the effects of water
immersion on neural activity, including somatosensory processing. To this end, we examined the effect of water
immersion on short-latency somatosensory evoked potentials (SEPs) elicited by median nerve stimuli. Short-latency
SEP recordings were obtained for ten healthy male volunteers at rest in or out of water at 30C. Recordings were
obtained from nine scalp electrodes according to the 10-20 system. The right median nerve at the wrist was
electrically stimulated with the stimulus duration of 0.2 ms at 3 Hz. The intensity of the stimulus was fixed at
approximately three times the sensory threshold.
Results: Water immersion significantly reduced the amplitudes of the short-latency SEP components P25 and P45
measured from electrodes over the parietal region and the P45 measured by central region.
Conclusions: Water immersion reduced short-latency SEP components known to originate in several cortical areas.
Attenuation of short-latency SEPs suggests that water immersion influences the cortical processing of
somatosensory inputs. Modulation of cortical processing may contribute to the beneficial effects of aquatic therapy.
Trial Registration: UMIN-CTR (UMIN000006492)
Background
Water immersion activates several distinct somatosen-
sory modalities, including tactile, pressure, and thermal
sensations. Somatosensory inputs can induce a variety of
cardiovascular and respiratory responses, including
decreased heart rate, increased stroke volume 1, and
reduced functional residual capacity 2. These physiolo-
gical responses can have therapeutic benefits; indeed,
water immersion is used as part of rehabilitation
regimes for orthopedic, cardiovascular, and respiratory
disorders. Water immersion once a week also improved
the activities of daily living (ADL) in some frail elderly
and hemiplegic patients after stroke 3. Benefits to neu-
rological patients suggest that water immersion may
influence cerebrocortical processing, but this remains to
be determined. Elucidating the cortical somatosensory
processes induced by water immersion and the effects of water immersion on the processing of other sensory
inputs will help delineate t
he mechanisms of sensory
integration and could facilitate the development of
improved aquatic therapies for neurology patients. Somatosensory input from peripheral nerves activates
several cortical areas. This modulation of somatosen-
sory input can be evaluated by somatosensory-evoked
potentials (SEPs). SEPs are divided into short-latency
and long latency types. Short-latency SEPs (with laten-
cies of 20 to 40 ms) are generated in area 3b andor
area 1 during thalamocortical inputs 4 and reflect the
first stage of cortical somatosensory processing. Many
reports have shown that somatosensory input attenu-
ates short-latency cortical SEPs evoked by median
nerve stimuli in the cerebral cortex or in the subcorti-
cal structures during movement 5,6 and in the pre-
sence of interfering tactile stimuli 7,8. In 1981, Jones
et al. 9 investigated whether short-latency SEPs
evoked by median nerve sti muli were affected by var-
ious interfering tactile st imuli, and proposed that
short-latency SEPs could be influenced by light touch
* Correspondence: daisuke@nuhw.ac.jp1Institute for Human Movement and Medical Sciences, Niigata University of
Health and Welfare, Shimami- cho 1398, kita-ku, Niigata city, Japan, 950-3198
Full list of author information is available at the end of the article
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2012 Sato et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http:creativecommons.orglicensesby2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.

stimuli of the body. In scalp recordings, continuous
interfering tactile stimuli applied to the median nerve
distribution of the hand primarily affected early SEP
components peaking at about 20-30 ms, inverting the
polarity between the parietal and frontal regions 7,10.
Subsequently, Jones et al. 8 showed that short-latency
SEPs generated in somatosensory cortical areas 3b and
1 were attenuated by interfering tactile stimuli and
cutaneous pressure 8. Based on these studies, it
appears that somatosensory inputs evoked by water
immersion, such as the tactile sense of water and
hydrostatic pressure, may affect the short-latency SEPs
generated in areas 3b and 1.In our previous study usin g functional near infrared
spectroscopy (fNIRS), water immersion was associated
with increased oxygenated hemoglobin (oxyHb) con-
centrations within the sensorimotor area of the cortex,
including areas 3b and 1. This finding suggests that
the somatosensory input from water immersion might
activate this cortical area 11. However, to the best of
our knowledge, there is no direct evidence that water
immersion has any effect on somatosensory cortical
processing. In the present study, we examined the
effect of water immersion on the short-latency SEPs in
response to median nerve stimuli. Based on the afore-
mentioned results, we hypothesized that somatosensory
inputs from water would attenuate these short-latency
SEPs.
Results
Figure 1 presents the grand average SEP waveforms
from all ten subjects. We measured the amplitudes of
P20, N30, and P45 from electrodes F3 and Fz, N18, P22,
N30, and P45 from electrodes C3 and Cz, and N20, P25,
N33, and P45 from electrodes P3 and Pz. Each SEP
component was identified by unique latency, polarity,
and scalp distribution and each was consistently
recorded in all subjects. Table 1 shows the amplitudes and latencies of these
SEP components under nonimmersed control and
immersed conditions. Results of a two-factor repeated
measures ANOVA revealed no significant interaction
between conditions (control or immersed) and the spe-
cific electrode on the amplitude of these SEP compo-
nents. There was a significant main effect of condition
in the parietal region (P25: F(1,9) = 16.03, P 0.01; P45:
F(1,9) = 10.21, P 0.05) and in the central region (P45:
F(1,9) = 12.51, P 0.01). Tukeys post hoc tests revealed
significant effects of immersion on the P45 amplitude
measured by the central electrodes C3 and Cz, and on
P25 and P45 amplitudes meas ured by the parietal elec-
trodes P3 and Pz. In contrast, the P20, N30, and P45
amplitudes measured by the F3 and Fz electrodes were
not significantly different between nonimmersed control and immersed conditions. Similarly, the N18, P22, and
N30 amplitudes measured by the C3 and Cz electrodes
were not significantly different between the nonim-
mersed control and immersed conditions. Finally, the
N20 and N33 amplitudes measured by P3 and Pz elec-
trodes were not significantly altered by water immer-
sion. Results of the two-factor repeated measures
ANOVA revealed no signifi
cant interaction between
condition and electrode on the latency of any SEP com-
ponent, and no significant main effect of experimental
condition on the all electrodes.
Discussion
Water immersion has been shown to benefit many
patients, including patients recovering from stroke, sug-
gesting that this form of therapy might alter cortical
activity. In the present study, such an effect was directly
demonstrated under controlled experimental conditions.
Water immersion significantly attenuated short-latency
SEPs evoked by median nerve stimuli. While the ampli-
tudes of the central N18, P22, and N30, the frontal P20
and N30, and the parietal N20 and P33 components
were not changed significantly by water immersion, the
parietal P25 and P45 amplitudes as well as the central
P45 amplitude were significantly smaller under the
immersed condition. These results suggest that water
immersion has a gating effect on short-latency SEPs
evoked by median nerve stimuli, and can therefore influ-
ence the cortical processing of somatosensory inputs.
Figure 1 Grand averaged short-latency components of the SEP
waveforms from each electrode . P20, N30, and P45 were
measured by electrodes F3 and Fz (top panel), N18, P22, N30, and
P45 by electrodes C3 and Cz (middle panel), and N20, P25, N33, and
P45 by electrodes P3 and Pz (lower panel). Black lines are the grand
averaged waveforms under nonimmersed control conditions from
the 10 subjects. Grey lines are the grand averaged waveforms
during water immersion.
Sato
et al.BMC Neuroscience 2012,13:13
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Water immersion can alter numerous physiological
parameters depending on physical characteristics like
buoyancy, hydrostatic pressure, and temperature. Water
immersion can provide relief from edema and improve
blood flow 12,13, and these effects are beneficial for
the rehabilitation of patients with orthopedic 14, cardi-
ovascular 15, or respiratory disorders 16. On the
other hand, the effects of water immersion on somato-
sensory cortical processing have never been examined,
despite the fact that water immersion is a form of multi-
modal somatosensory stimulation, engaging tactile-,
pressure-, and thermosensi tive pathways, and so would
be expected to evoke widespr ead cortical activity. The
present results provide a foundation for further studies
on the benefits of aquatic rehabilitation for frail elderly
and patients with neurological disorders, such as hemi-
plegic stroke patients. Somatosensory inputs can attenuate short-latency
SEPs evoked by other inputs, most often stimulation of
the median nerve 5,7,9,10,17. Jones et al. 8 demon-
strated that interfering tact ile stimuli, such as continu-
ous rubbing of the palm ipsilateral to the median nerve,
attenuated P25 and P29 due to centripetal gating. Acu-
puncture and tactile stimulation with a soft nylon brush
to the ipsilateral palm also attenuated the parietal P22
(corresponding to P25) evoked by median nerve stimuli
18. The author 18 suggested that the suppression of P22 is due to a uniform decrease in neuronal activity
within the somatosensory area due to
afferent inhibi-
tion 19.
We were uncertain why attenuation of the P25 com-
ponent occurred in the present study under immersion
conditions, since the hand that was innervated by the
median nerve was not actually in the water. According
to an earlier study 7 that examined changes in the
waveform of SEPs due to continuous tactile stimuli to
various parts of the body, including the face, hand, fore-
arm, and foot both ipsilateral and contralateral to the
median nerve stimuli, tactile stimuli of remote regions
resulted in a consistent dif ference in the waveforms of
short-latency SEPs. The authors proposed that this may
be analogous to the phenomenon of surround inhibi-
tion described by Mountcastle and Powell 19 in
which single unit responses were observed in the sen-
sory cortex of the monkey. Additionally, they suggested
that all areas of the skin may influence the cortical
responses induced by median nerve stimuli. Therefore,
somatosensory input from the whole of the body while
immersed in water may have re sulted in attenuation of
the P25 component in the present study, but further
studies are necessary to confirm this possibility and
determine the underlying mechanisms. The mapped P25 field is always confined to the con-
tralateral parietal scalp and is thought to reflect
Table 1 Mean amplitudes and latencies of the SEP components (SE)
amplitude( V) latency (ms)
Electrode Component Nonimmersed Immersed Nonimmersed Immersed
Fz P20 0.90 (0.12) 0.89 (0.12) 20.30 (0.54) 20.60 (0.62) N30-2.21 (0.38) -2.27 (0.36) 32.20 (1.61) 32.20 (1.73)
P45 1.85 (0.33) 1.58 (0.26) 47.90 (0.66) 47.30 (0.86)
F3 P201.09 (0.16) 0.98 (0.13) 20.40 (0.22) 20.50 (0.27)
N30 -2.17 (0.39) -1.92 (0.35) 30.90 (1.18) 30.20 (1.49)
P45 2.09 (0.40) 1.67 (0.31) 46.40 (1.36) 46.00 (1.05)
Cz N18-0.79 (0.17) -0.97 (0.27) 18.60 (0.60) 19.10 (0.84)
P22 0.62 (0.10) 0.70 (0.20) 23.00 (0.99) 22.70 (1.07)
N30 -1.49 (0.27) -1.52 (0.26) 32.20 (0.93) 32.30 (0.78)
P45 2.16 (0.23) 1.70 (0.19) 47.00 (1.04) 45.50 (0.86)
C3 N18-1.29 (0.16) -1.24 (0.18) 18.80 (0.29) 18.70 (0.30)
P22 2.11 (0.32) 1.99 (0.29) 23.60 (0.54) 23.30 (0.50)
N30 -1.88 (0.38) -1.94 (0.38) 30.70 (0.33) 30.80 (0.47)
P45 2.90 (0.31) 2.68 (0.31) 46.70 (1.30) 45.00 (1.30)
Pz N20-1.33 (0.14) -1.42 (0.12) 19.60 (0.34) 20.25 (0.35)
P25 1.23 (0.20) 1.02 (0.21) 23.80 (0.49) 24.25 (0.60)
N33 -1.20 (0.14) -1.19 (0.11) 31.20 (0.59) 30.88 (0.68)
P45 1.52 (0.18) 1.36 (0.19) 43.70 (1.34) 41.88 (0.86)
P3 N20-1.96 (0.23) -1.98 (0.24) 19.70 (0.21) 19.70 (0.15)
P25 2.13 (0.31) 1.83 (0.34) 24.40 (0.70) 24.20 (0.63)
N33 -1.33 (0.19) -1.22 (0.18) 31.40 (0.64) 31.50 (0.60)
P45 1.92 (0.22) 1.74 (0.24) 42.20 (1.01) 41.10 (0.77)
Sato
et al.BMC Neuroscience 2012,13:13
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activation in the various somatosensory receiving areas
20. Indeed, patients with complete parietal vascular
lesions and hemianesthesia lost both N20 and P25 21.
Desmedt and Tomberg 22 examined the topographical
patterns of short-latency SEPs and proposed that P27,
which corresponds to P25 in the present study, reflects
radially oriented neural generators in parietal area 1.
Short-latency (20-40 ms) responses are generated mainly
in areas 3b and 1 of the contralateral SI 23. In a pre-
vious study that examined intracortical connectivity to
the afferent input from skin in monkeys, area 1 was
shown to receive a direct thalamocortical projection
from the VPLc, as well as a corticocortical projection
from area 3b 24. According to a functional magnetic
resonance imaging (fMRI) study, activity in areas 3 and
1 increased when pressure without pain was applied to
the fingertip and antebrachial regions 25. Therefore,
the attenuation of P25 in the present study suggests that
the somatosensory input from the immersed area of
skin could alter excitability in areas 3b and 1. The P45 field is inconsistent in young adults and its
distribution over the scalp is quite variable. It always
involves the contralateral central region, but can also
extend over the front of the scalp 20. This is in agree-
ment with the present resu lts, as 40-50 ms responses
were found at all electrodes. Furthermore, P45 was
recorded precentrally in a patient with complete
destruction of the parietal cortex 21; therefore, the P45
generator cannot be uniquely parietal. The attenuation of P45 in the present study could be
explained due to several cortical activities which were
induced by the somatosensory input from water. Kawa-
shima et al. 18 reported that attenuation of P40 (which
corresponds to P45 in the p resent study) was induced
by interfering tactile stim uli. They suggested that the
generator of P40 is area 2 based on the dipole tracing
method. However, others have proposed that the gen-
erator of P45 is located in SI 26. As described above,
although the generator of P45 is still unknown, it is pos-
sible that P45 reflects activity in the SI. Therefore,
somatosensory input to the SI as the result of water
immersion might induce the attenuation of P45. An added possible explanation for the attenuation of
P45 involves that there is an effect from activity in the
PPC. Mauguiere et al. 21 proposed that P45 in healthy
adults could reflect activity in several areas of the parie-
tal cortex, including SI and the PPC. Inui et al. 27
investigated the temporal relationship among cortical
responses to somatosensory stimuli using magnetoence-
phalography (MEG) and found that the activities peak-
ing at 29 and 37 ms were located in the postcentral
gyrus, corresponding to the PPC. Although a few MEG
studies reported activation in this area at a latency of
50-100 ms following somatose nsory stimuli 28,29, themain inputs to this area are from areas 1 and 2 in maca-
que monkeys 30. Therefore, somatosensory input from
water immersion to the PPC via SI might lead to the
attenuation of P45. Furthermore, Inui et al. 27 pro-
posed a hierarchical scheme of somatosensory proces-
sing from area 3b (peaking at 21-30 ms) to area 1
(peaking at 25-34 ms) and the PPC (peaking at 29-37
ms). Therefore, the attenuations of P25 (peaking at 23-
30 ms) and P45 (peaking at 37-46 ms) in the present
study might indicate a hierarchical processing from area
SI to PPC of somatosensory input induced by water
immersion.
The other possible explanation for the attenuation of
P45 assumes that there is an effect from activity in the
supplementary motor area (SMA) as well as the SI. The
SMA does not appear to receive direct somatosensory
input from the thalamus, but in monkeys it does receive
projections from SI, SII, and area 5. Some neurons in
the SMA respond to mechanical stimuli, such as light
pressure or limb displacement 31. Furthermore, Bode-
gard et al. 32 used fMRI in humans to show that light
pressure to the index finger increased SMA activation.
Additionally, a 40 ms positive potential was generated in
a hand representation of the SMA 23. Since afferent
inputs are transmitted to the SMA via SI and the PPC
33, the present results cannot rule out this possibility.
Conclusion
We demonstrated that water immersion modulates the
short-latency SEPs known to originate in the SI. We
propose that attenuation of short-latency SEPs is caused
by somatosensory inputs from water, and that water
immersion influences the cortical processing of other
somatosensory inputs.
Methods
Subjects
Somatosensory-evoked potential (SEP) recordings were
obtained in ten healthy male volunteers age 20-30 years
(mean age, 21.8 2.5 years) who gave their informed
consent before the study commenced. All subjects were
right-handed, none had a history of neurological or psy-
chiatric disease, and none were taking any medications.
The present study was performed in accordance with
the Declaration of Helsinki and approved by the local
ethical committee.
SEPs recordings and stimulus
The subjects wore only swimwear and were seated on a
comfortable reclining armchair with a mounted headrest
surrounded by shielding cur tain to prevent electrical
interference. They were instructed to relax during the
SEP measurements and to ignore the stimulus. A
SynAmps amplifier system controlled by Scan 4.3
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software (Neuroscan, El Paso, TX, USA) was used to
record EEG data. A 32-electrode Neuroscan Quickcap
based on the 10-20 system was positioned on the sub-
ject s head, and conducting gel was applied to each elec-
trode to establish and maintain scalp contact.
Recordings were obtained from nine scalp electrodes
placed at F3F4, C3C4, P3P4, Fz, Cz, and Pz. All of
the scalp electrodes were referenced to linked earlobe
electrodes. Electrode impedances were kept below 5 k .
The sampling rate was 1,000 Hz. The right median nerve at the wrist was electrically
stimulated with 0.2 ms pulses at 3 Hz using a conven-
tional bipolar felt-tipped electrode. The intensity of the
stimulus (7.4 2.3 mA) was fixed at about three times
the sensory threshold (mean, 2.5 0.7 mA). Stimulus
intensity was always below the pain threshold for each
subject.
Conditions
The SEPs were measured while they were at rest both in
and out of water. The subjects maintained the same
body position under both immersed and nonimmersed
control conditions. The entire experiment required 30
min, including the preparation time (Figure 2). Measure-
ments under immersed conditions began immediately
after water immersion. For the nonimmersed control
measurements, the ambient temperature was set at 30
C, while for immersed SEP measurements, both ambient
and water temperatures were set at 30C. Water was
poured up to the axillary level of each subject. The right
hand was placed on the armchair above the water level
with the proximal portion of the right arm immersed in
water (Figure 3). To avoid carryover effects, SEP mea-
surements under nonimmersed control and immersed
conditions were performed in random order.
SEP analysis
All data were stored in a personal computer, and signal
processing software (NeuroScan) was used for analysis.
The continuous EEG was segmented into epochs of 70
ms that included a 10 ms prestimulus period. Before
averaging, each epoch underwent correction of slow lin-
ear trends by high-pass filtering and baseline correction
using the prestimulus period. A high-pass filter (1 Hz, 6
dBoct) was applied, together with a 50 Hz notch filter. Epochs were visually inspected and rejected from the
average if voltage variations exceeded 70
V. The
remaining data ( 500 epochs) were averaged.
The amplitudes of P20, N30, and P45 measured at elec-
trodes F3 and Fz, N18, P22, N30, and P45 measured at
electrodes C3 and Cz, and N20, P25, N33, and P45 mea-
sured at electrodes P3 and Pz were identified on the basis
of their latency, polarity, and scalp distribution. The peak
amplitude of the SEPs was referenced to the peak of the
preceding response. The peak amplitudes of the first
components were defined from baseline-to-peak. The
latencies were measured from stimulus onset to the peak
of each component. The amplitudes and latencies of all
components measured at all electrodes were analyzed by
a two-factor repeated measures ANOVA for condition
and electrode, and Tukey sposthoctestswereusedfor
pair-wise comparisons. If the assumption of sphericity
was violated in Mauchly s sphericity test, the degree of
freedom was corrected using Greenhouse-Geisser scor-
rection coefficient epsilon, and F- and P- values were
recalculated. The significance level was set at 5%.
List of abbreviations
SEP: somatosensory evoked potential; fMRI: functional magnetic resonance
imaging; SI: primary somatosensory area; PPC: posterior parietal cortex; SMA:
supplementary motor area.
Acknowledgements
This study was supported by a Grant-in-Aid for Young Scientists (B) from the
Ministry of Education, Culture, Sports, Science and Technology (MEXT) of
Japan. It was also supported by a Grant-in-Aid for Advanced Research from
the Niigata University of Health and Welfare.
Author details
1Institute for Human Movement and Medical Sciences, Niigata University of
Health and Welfare, Shimami- cho 1398, kita-ku, Niigata city, Japan, 950-3198.
2Department of Health and Sports, Niigata University of Health and Welfare,
Shimami- cho 1398, kita-ku, Niigata city, Japan, 950-3198.3Department of
Physical Therapy, Niigata University of Health and Welfare, Shimami- cho
1398, kita-ku, Niigata city, Japan, 950-3198.Figure 2 The experimental procedure in the present study .
During the preparation period, we confirmed electrode impedances,
water and ambient temperature, and body position of the subject.
Figure 3 The experimental setup used to measure SEPs under
nonimmersed control and immersed conditions .
Sato
et al.BMC Neuroscience 2012,13:13
http:www.biomedcentral.com1471-22021313 Page 5 of 6

Authorscontributions
DS conceived of the experiment and was the primary investigator involved
in the data collection and analysis as well as drafting of the manuscript. KY,
HO, and AM (senior author) contributed to the experimental design, data
analysis, and manuscript editing. YS contributed to manuscript editing. YT
contributed to the data collection. All authors read and approved the final
manuscript.
Received: 25 August 2011 Accepted: 24 January 2012
Published: 24 January 2012
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doi:10.11861471-2202-13-13
Cite this article as: Satoet al.:The effect of water immersion on short-
latency somatosensory evoked potentials in human. BMC Neuroscience
2012 13:13.
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