August 2001
Volume 42, Issue 9
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Physiology and Pharmacology  |   August 2001
Sensations Evoked by Selective Mechanical, Chemical, and Thermal Stimulation of the Conjunctiva and Cornea
Author Affiliations
  • M. Carmen Acosta
    From the Instituto de Neurociencias, Universidad Miguel Hernández-Consejo Superior de Investigaciones Cientificas (CSIC), Campus de San Juan, San Juan de Alicante, Spain; and the
  • Maxine E. Tan
    Cooperative Research Centre of Eye Research and Technology, University of New South Wales, Sydney, Australia.
  • Carlos Belmonte
    From the Instituto de Neurociencias, Universidad Miguel Hernández-Consejo Superior de Investigaciones Cientificas (CSIC), Campus de San Juan, San Juan de Alicante, Spain; and the
  • Juana Gallar
    From the Instituto de Neurociencias, Universidad Miguel Hernández-Consejo Superior de Investigaciones Cientificas (CSIC), Campus de San Juan, San Juan de Alicante, Spain; and the
Investigative Ophthalmology & Visual Science August 2001, Vol.42, 2063-2067. doi:
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      M. Carmen Acosta, Maxine E. Tan, Carlos Belmonte, Juana Gallar; Sensations Evoked by Selective Mechanical, Chemical, and Thermal Stimulation of the Conjunctiva and Cornea. Invest. Ophthalmol. Vis. Sci. 2001;42(9):2063-2067.

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Abstract

purpose. To study the sensations evoked by selective mechanical, chemical, and thermal stimulation of the conjunctiva and compare them with those elicited by similar stimulation of the cornea.

methods. Six young subjects participated in the study. Using a gas esthesiometer, selective mechanical (air puffs at flows from 0 to 264 ml/min), chemical (0–80% CO2 in air), and thermal (air at temperatures from −10°C to +80°C) stimulation was performed on the center of the cornea and on the temporal conjunctiva. The intensity, degree of irritation, stinging and burning pain components, and thermal characteristics of the evoked sensation were evaluated after each stimulus in separate, 10-cm continuous visual analogue scales (VASs). The ability of the subjects to identify the quality of the stimulus applied to the cornea and the conjunctiva was also studied.

results. The subjective intensity and thermal components (cooling or warming) of the sensation reported after mechanical, chemical, and heat stimulation were similar in the conjunctiva and cornea, although lower VAS scores were always reported in the conjunctiva for the irritation and the stinging and burning pain components. In the cornea, stimulation with low temperatures was perceived as a cooling sensation with an irritative component. In the conjunctiva, cooling was perceived as a purely cold sensation. Subjects showed similar discrimination capability in the cornea and the conjunctiva for the various types of stimuli.

conclusions. Sensations evoked in the cornea by selective mechanical, chemical, and heat and cold stimulation always presented an irritation component. In the conjunctiva, stimuli of the same intensity are always perceived as less irritating than in the cornea. Cold and other non-noxious subqualities of sensation can be evoked in the conjunctiva.

The quality of sensations arising from the application of different types of stimulating energy to the anterior surface of the eye has been a matter of discussion since von Frey’s pioneering studies on ocular sensitivity. 1 2 3 4 5 6 In the human cornea it has generally been assumed that application of mechanical, chemical, and thermal forces elicits only sensations of irritation and pain, 3 4 5 6 whereas in the bulbar conjunctiva, innocuous sensations of temperature could also be evoked by thermal stimulation. 3 However, in most of these studies the stimulation procedures precluded selective application of a given form of energy and a precise control of the stimulation parameters, thus making it difficult to define the site of origin of the sensation and its psychophysical characteristics. 
A more accurate procedure for stimulating the ocular surface was recently made available by the gas esthesiometer, 7 an instrument that allows the delivery of gas pulses of controlled mechanical force, temperature, and varying CO2 concentration to the ocular surface. In humans, application with the gas esthesiometer of mechanical force, noxious heat, and low pH to the cornea evokes unpleasant sensations, with the degree of irritation, quality of pain, and thermal characteristics varying with the modality of stimulus. In contrast, moderate cold stimulation of the cornea elicits an innocuous sensation of cooling that becomes irritating when low temperatures are achieved. 8 In the human conjunctiva, a similar study of the sensations evoked by selective application of different modalities of stimuli has not been performed. In the present work, the psychophysical characteristics of the sensations elicited by mechanical, thermal, and chemical stimulation of the bulbar conjunctiva with the gas esthesiometer were analyzed in human subjects and compared with those obtained from the cornea. Preliminary results have been published in abstract form. 9  
Materials and Methods
Subjects
Three women and three men were included in the study (mean age, 23.8 ± 0.6 years). They received financial compensation for their participation. The research followed the tenets of the Declaration of Helsinki. The subjects signed an informed consent to a protocol approved by our institute and were free to interrupt the session at any time. None of them had a history of corneal or ocular disease. Three wore eyeglasses to correct myopia (less than −2 diopters [D]). Selective mechanical, chemical, and thermal stimulations of the cornea and the conjunctiva were performed in both eyes. The protocol was completed on four separate days. 
Esthesiometry
A gas esthesiometer previously described 7 was used to apply to the corneal or conjunctival surface 3-sec gas jets of adjustable flow, composition, and temperature, separated by 2-minute pauses. Selective mechanical stimulation consisted of a series of nine pulses of air at variable flow (0–264 ml/min) heated to 50°C at the tip of the probe to prevent changes in the temperature of the ocular surface during the air puff. A series of nine pulses of air and CO2 mixture of different concentrations (0–80% CO2) at 50°C and with a flow 6.25 ml/min below mechanical threshold was used for chemical stimulation. Thermal (heat and cold) stimulation was performed by applying to the cornea and conjunctiva 10 pulses of air at different temperatures (−10°C to+ 80°C), which produced variations of the basal corneal temperature (34.4°C) of −5°C to +3°C (see Refs. 7 and 8 ) at a flow rate 6.25 ml/min below mechanical threshold. In all experiments, pulses of different intensity were applied randomly. Mechanical threshold was determined using the method of levels. 10 Sensation threshold for chemical and thermal stimulation was determined with the method of minimum stimulus, that is, the lowest intensity of stimulus that evoked a response of 0.5 VAS units or more. 8  
The esthesiometer probe was located in a slit lamp table and its tip was placed at a distance of 5 mm from the ocular surface measured with a transparent ruler, perpendicular to the center of the cornea or the temporal conjunctiva (5 mm from the limbus). The subject was asked to blink immediately before the onset of each stimulus, which was identified by the click produced by the opening of a valve inside the probe. Immediately after each individual stimulus, the subject evaluated sequentially, in six separate, continuous, horizontal VASs, the components of the sensation experienced (intensity, irritation, stinging and burning components of the irritation, and warming or cooling thermal components). Intensity–response curves for the various parameters of the sensation were subsequently made. 7 8  
The ability of the subjects to identify the type of stimulus applied to the cornea and the conjunctiva was also evaluated in a separate group of experiments. Mechanical, chemical, and hot and cold stimuli of the same subjective intensity (3 VAS units) were randomly applied twice to both eyes. The conjunctiva and the cornea were explored in separate sessions. Subjects were asked to identify the quality of the stimulus that had been delivered, based on the experience obtained in a previous stimulation series in which the different types of stimuli were identified and applied immediately afterward. 
Data were expressed as mean ± SEM of the values from the six subjects (both eyes) in whom corneal and conjunctival responses were determined. Pearson product moment correlation was performed to measure the association between the intensity of the stimulus and the response of subjects (VAS values). If the correlation was significant (P < 0.05), the dependence of VAS scores on the intensity of the stimulus was predicted using linear regression. Slopes of linear regression lines were compared, to find differences between corneal and conjunctival responses. 
Results
Threshold of the Sensation
Table 1 presents the mean threshold values for mechanical, thermal, and chemical stimulation of the cornea and the conjunctiva. No significant differences in threshold for any of the stimuli were found between the cornea and the conjunctiva. 
Mechanical Stimulation
In the conjunctiva and the cornea, a positive, significant correlation was found between the magnitude of the stimulus and the VAS score for subjective intensity. Moreover, VAS scores for equivalent stimuli in both structures overlapped (Fig. 1A) . The VAS scores for irritation (Fig. 1B) and stinging (Fig. 1C) and burning pain (Fig. 1D) also correlated significantly with the magnitude of the stimulus. However, the scores for these parameters of sensation were comparatively lower in the conjunctiva than in the cornea, as was reflected in the slope of the respective stimulus–response curves (Figs. 1B 1C 1D , insets). VAS scores for cooling and warming sensations associated with mechanical stimulation of the cornea and conjunctiva were similar (Figs. 1E 1F)
Chemical Stimulation
The intensity of the sensation evoked by increasing CO2 concentrations reached similar levels in the cornea and the conjunctiva, and correlated significantly with the percentage of CO2 in the gas mixture (Fig. 2A) . Scores for irritation and its burning pain component also correlated with the intensity of the stimulus (Figs. 2B 2D) and were lower in the conjunctiva than in the cornea (Figs. 2B 2D , insets). Stinging pain and the warming and cooling components evoked by chemical stimulation were of similar magnitude in both tissues (Figs. 2C 2E 2F)
Thermal Stimulation
Heat.
VAS scores for the intensity of the sensation evoked by hot air increased monotonically with the temperature of the stimulus and were similar on the cornea and the conjunctiva (Fig. 3A , right side of the curve). The degree of irritation and the stinging and burning pain sensations produced by hot stimuli were slightly lower in the conjunctiva (Figs. 3B 3C 3D , right side). VAS scores for the warming and cooling components of the sensation evoked by heat were similar in the cornea and the conjunctiva (Figs. 3E 3F ; right side of the curve). 
Cold.
Scores for intensity of the sensation evoked by cold air were similar in the cornea and in the conjunctiva (Fig. 3A , left side of the curve). In contrast, VAS scores for irritation and for its stinging component were lower in the conjunctiva than in the cornea (Figs. 3B 3C , left side). Warming and cooling components of the sensation evoked by cold air were similar in the cornea and in the conjunctiva (Figs. 3E 3F , left side). 
Correlation between the Different Components of the Sensations
In Figure 4 , the intensity–response curves for the parameters intensity and irritation were represented together, to examine for associations between intensity detection and unpleasantness of the sensations evoked by the different stimulus modalities. 
It is apparent that in the cornea, curves for intensity detection and for irritation induced by mechanical forces, CO2, and heat overlapped, suggesting that subjects did not discriminate well between the intensity of the sensation and the degree of irritation evoked by the same stimulus (Figs. 4A 4B 4C , left). In the case of cold stimulation, curves representing the intensity and the cooling component also overlapped, whereas irritation was noticeable only at low temperatures (Fig. 4C , left). 
In contrast, in the case of the conjunctiva the curves of intensity and irritation obtained by mechanical stimulation did not overlap (Fig. 4A , right), suggesting that in this tissue, partially separated neural pathways are used to signal innocuous mechanical stimuli and pain (see the Discussion section), whereas for chemical and hot stimulation, intensity–response curves for the parameters intensity and irritation overlapped, indicating a common neural pathway. Low-temperature stimuli produced a distinct sensation of cooling devoid of an irritative component (Figs. 4B 4C , right). 
Identification of the Type of Stimulus
Table 2 presents the percentage of correct identifications of the type of stimulus applied to the cornea and the conjunctiva. The ability of subjects to identify the quality of stimuli with the same subjective intensity was high and similar in both structures. Chemical and hot stimuli were slightly less accurately identified in the conjunctiva than in the cornea. 
Discussion
This study demonstrates that selective stimulation of the cornea and the bulbar conjunctiva with controlled mechanical, chemical, and thermal stimuli evoked sensations whose subjective intensity was proportional to the magnitude of the applied stimulus. Furthermore, the results show that the quality of the sensations evoked by these stimuli, measured in terms of the ratings given to the various parameters that defined the sensation, were distinguishable and different for the cornea and for the conjunctiva. This confirms that psychophysical direct magnitude scaling methods are useful to evaluate the magnitude and dimensions of pain sensations arising from the ocular surface, as it has been convincingly demonstrated for pain evoked by experimental stimulation of the skin. 11 12  
Previous reports on conjunctival and corneal sensitivity were largely limited to the determination of mechanical thresholds and included only incidental comments about the quality of the evoked sensation. 2 3 4 5 13 14 15 16 17 With the Cochet-Bonnet esthesiometer, mechanical threshold values were markedly lower in the cornea than in the conjunctiva, in which large regional variations in sensitivity have been additionally reported. 14 15 Differences in mechanical threshold between cornea and conjunctiva were less pronounced when a pneumatic esthesiometer using air at room temperature was used. 17 In the present experiments, in which mechanical threshold was determined with a jet of warmed gas that prevented cooling of the ocular surface, no differences in threshold were found between tissues. The discrepancy in mechanical thresholds obtained with the different instruments possibly reflect a variable recruitment of the various types of corneal and conjunctival sensory afferents. Although all procedures are expected to stimulate thin myelinated and unmyelinated polymodal sensory fibers, touching the cornea with the Cochet-Bonnet esthesiometer fully activates Aδ mechanosensory fibers, 18 which are important for the production of a sensation of sharp pain and this population, seems to be poorly recruited by mechanical stimulation with a gas jet. 8 Moreover, the higher innervation density of the cornea in comparison with the conjunctiva may be important in detecting a punctate stimulus performed with a hair, but may be less critical when a larger surface is stimulated, as occurs with a gas jet. Finally, a variable recruitment of cold-sensitive fibers in the cornea and the conjunctiva by the gas esthesiometers may be the reason for the small differences in detection thresholds obtained with these instruments. 8 17  
In the cornea, the intensity and irritation curves of the sensation evoked by mechanical stimulation overlapped, whereas in the conjunctiva, mechanical stimuli of low and moderate magnitude had a very low irritation component, although their intensities were clearly detected. These observations suggest that the conjunctiva, unlike the cornea, contains low-threshold mechanoreceptor afferent nerves 19 that are initially activated by stimuli of weak intensity that evoke innocuous sensations, in addition to the presence of nociceptor fibers, whose recruitment by higher intensity stimuli produce irritation and pain. 20 They further confirm that in the cornea mechanical stimuli are encoded exclusively by sensory afferent nerves of the nociceptor type. 8  
Differences in the subjective intensity and irritation response curves were not apparent when stimulation was performed with CO2, a stimulus that recruits mainly polymodal sensory fibers, 6 evoking intensity and irritation response curves that overlapped completely, both for the cornea and the conjunctiva. VAS scores were comparatively lower in the case of the conjunctiva, possibly because the decrease in pH caused by CO2 is more effectively buffered in the richly vascularized conjunctival tissue than in the cornea. 
Low-temperature stimuli of moderate intensity provoked purely cold sensations in the conjunctiva and the cornea. In the cornea, more pronounced temperature declines also elicited irritation and pain. 3 8 These unpleasant sensations were not evoked by comparable stimuli in the conjunctiva, in which lower VAS scores than in the cornea were also reported in response to similar cold stimuli. This suggests that in the conjunctiva, as seems to occur in the cornea, moderate temperature changes caused by the cooled air jet activates exclusively thermal receptor endings sensitive to cold, 21 which evokes innocuous thermal sensations. 3 Presumably, in the conjunctiva temperature reductions caused by cold air are less pronounced than in the cornea, because of the attenuation of temperature changes by the blood flow. Accordingly, a local temperature decrease may be insufficient to activate conjunctival polymodal nociceptors, as in the cornea, when extreme cold is applied. 8 Moreover, the lower density of polymodal nociceptive fibers in the conjunctiva reduces the probability of recruitment of nociceptive endings by intense cooling. 
Positive identification of the modality of the applied stimulus was made for the cornea and the conjunctiva. This is in agreement with the observations made by Kenshalo 3 of pure thermal sensations arising from the conjunctiva and confirms those of Acosta et al. 8 in the cornea, where the presence of thermal sensations has been a matter of discussion for years. 2 3 4 5 8 Furthermore the present results support the interpretation that the final subquality of sensations arising from the ocular surface is determined by simultaneous activation of different populations of sensory afferents. When polymodal nociceptive fibers are activated, subjects experience a blended sensation that possesses an identifiable quality but is dominated by an irritation component. 
 
Table 1.
 
Sensation Threshold for Mechanical, Chemical, and Thermal Stimulation of the Cornea and Conjunctiva with a Gas Esthesiometer
Table 1.
 
Sensation Threshold for Mechanical, Chemical, and Thermal Stimulation of the Cornea and Conjunctiva with a Gas Esthesiometer
Sensation Threshold Cornea Conjunctiva
Mechanical (ml/min) 82.8 ± 13.8 84.9 ± 10.4
Chemical (% of CO2 in air) 21.0 ± 4.6 16.0 ± 4.0
Hot (°C) 1.4 ± 0.1 2.0 ± 0.1
Cold (°C) −2.5 ± 0.6 −2.3 ± 0.4
Figure 1.
 
VAS scores for the different components of the sensation evoked by selective mechanical stimulation of the cornea (▿) and conjunctiva (•). (A) Subjective intensity; (B) irritation; (C) stinging pain; (D) burning pain; (E) warming sensation; and (F) cooling sensation. Insets: Linear regression of the respective data. Thin line: cornea; thick line: conjunctiva.
Figure 1.
 
VAS scores for the different components of the sensation evoked by selective mechanical stimulation of the cornea (▿) and conjunctiva (•). (A) Subjective intensity; (B) irritation; (C) stinging pain; (D) burning pain; (E) warming sensation; and (F) cooling sensation. Insets: Linear regression of the respective data. Thin line: cornea; thick line: conjunctiva.
Figure 2.
 
VAS scores obtained for the different components of the sensation after selective chemical stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 2.
 
VAS scores obtained for the different components of the sensation after selective chemical stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 3.
 
VAS scores obtained for the explored components of the sensation after selective thermal stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 3.
 
VAS scores obtained for the explored components of the sensation after selective thermal stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 4.
 
Comparison between intensity (open symbols) and irritation (closed symbols) curves for mechanical (A), chemical (B), and thermal (C) stimulation of the cornea (triangles) and conjunctiva (circles). (C) VAS scores for the cooling component of the sensation (gray shading) are also plotted for their comparison with intensity scores.
Figure 4.
 
Comparison between intensity (open symbols) and irritation (closed symbols) curves for mechanical (A), chemical (B), and thermal (C) stimulation of the cornea (triangles) and conjunctiva (circles). (C) VAS scores for the cooling component of the sensation (gray shading) are also plotted for their comparison with intensity scores.
Table 2.
 
Percentage of Correct Identifications of the Type of Stimulus
Table 2.
 
Percentage of Correct Identifications of the Type of Stimulus
Sensation Evoked
Mechanical Chemical Hot Cold Sham Undefined
Mechanical 46 ± 10 13 ± 9 21 ± 12 21 ± 12 0 0
42 ± 10 21 ± 8 13 ± 4 17 ± 8 4 ± 4 0
Chemical 8 ± 5 71 ± 10 21 ± 10 0 0 0
13 ± 9 63 ± 17 17 ± 5 4 ± 4 4 ± 4 0
Hot 0 38 ± 13 58 ± 14 0 0 3 ± 3
21 ± 10 17 ± 8 50 ± 17 4 ± 4 8 ± 5 0
Cold 17 ± 11 17 ± 10 0 67 ± 12 0 0
8 ± 5 8 ± 5 4 ± 7 79 ± 10 0 0
Sham 0 8 ± 8 8 ± 8 0 83 ± 11 0
0 0 8 ± 5 0 92 ± 5 0
The authors thank Alfonso Perez-Vegara for his technical assistance and Adolfo Aracil for collaboration in the initial experiments. 
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Lele PP, Weddell G. Sensory nerves of the cornea and cutaneous sensibility. Exp Neurol. 1959;1:334–259. [CrossRef] [PubMed]
Kenshalo DR. Comparison of thermal sensitivity of the forehead, lip, conjunctiva and cornea. J Appl Physiol. 1960;15:987–991. [PubMed]
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Chen X, Gallar J, Pozo MA, Baeza M, Belmonte C. CO2 stimulation of the cornea: a comparison between human sensation and nerve activity in polymodal nociceptive afferents of the cat. Eur J Neurosci. 1995;7:1154–1163. [CrossRef] [PubMed]
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Draeger J. Corneal Sensitivity: Measurement and Clinical Importance. 1984; Springer-Verlag New York.
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Figure 1.
 
VAS scores for the different components of the sensation evoked by selective mechanical stimulation of the cornea (▿) and conjunctiva (•). (A) Subjective intensity; (B) irritation; (C) stinging pain; (D) burning pain; (E) warming sensation; and (F) cooling sensation. Insets: Linear regression of the respective data. Thin line: cornea; thick line: conjunctiva.
Figure 1.
 
VAS scores for the different components of the sensation evoked by selective mechanical stimulation of the cornea (▿) and conjunctiva (•). (A) Subjective intensity; (B) irritation; (C) stinging pain; (D) burning pain; (E) warming sensation; and (F) cooling sensation. Insets: Linear regression of the respective data. Thin line: cornea; thick line: conjunctiva.
Figure 2.
 
VAS scores obtained for the different components of the sensation after selective chemical stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 2.
 
VAS scores obtained for the different components of the sensation after selective chemical stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 3.
 
VAS scores obtained for the explored components of the sensation after selective thermal stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 3.
 
VAS scores obtained for the explored components of the sensation after selective thermal stimulation of the cornea (▿) and conjunctiva (•). Data are depicted as in Figure 1 .
Figure 4.
 
Comparison between intensity (open symbols) and irritation (closed symbols) curves for mechanical (A), chemical (B), and thermal (C) stimulation of the cornea (triangles) and conjunctiva (circles). (C) VAS scores for the cooling component of the sensation (gray shading) are also plotted for their comparison with intensity scores.
Figure 4.
 
Comparison between intensity (open symbols) and irritation (closed symbols) curves for mechanical (A), chemical (B), and thermal (C) stimulation of the cornea (triangles) and conjunctiva (circles). (C) VAS scores for the cooling component of the sensation (gray shading) are also plotted for their comparison with intensity scores.
Table 1.
 
Sensation Threshold for Mechanical, Chemical, and Thermal Stimulation of the Cornea and Conjunctiva with a Gas Esthesiometer
Table 1.
 
Sensation Threshold for Mechanical, Chemical, and Thermal Stimulation of the Cornea and Conjunctiva with a Gas Esthesiometer
Sensation Threshold Cornea Conjunctiva
Mechanical (ml/min) 82.8 ± 13.8 84.9 ± 10.4
Chemical (% of CO2 in air) 21.0 ± 4.6 16.0 ± 4.0
Hot (°C) 1.4 ± 0.1 2.0 ± 0.1
Cold (°C) −2.5 ± 0.6 −2.3 ± 0.4
Table 2.
 
Percentage of Correct Identifications of the Type of Stimulus
Table 2.
 
Percentage of Correct Identifications of the Type of Stimulus
Sensation Evoked
Mechanical Chemical Hot Cold Sham Undefined
Mechanical 46 ± 10 13 ± 9 21 ± 12 21 ± 12 0 0
42 ± 10 21 ± 8 13 ± 4 17 ± 8 4 ± 4 0
Chemical 8 ± 5 71 ± 10 21 ± 10 0 0 0
13 ± 9 63 ± 17 17 ± 5 4 ± 4 4 ± 4 0
Hot 0 38 ± 13 58 ± 14 0 0 3 ± 3
21 ± 10 17 ± 8 50 ± 17 4 ± 4 8 ± 5 0
Cold 17 ± 11 17 ± 10 0 67 ± 12 0 0
8 ± 5 8 ± 5 4 ± 7 79 ± 10 0 0
Sham 0 8 ± 8 8 ± 8 0 83 ± 11 0
0 0 8 ± 5 0 92 ± 5 0
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