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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 38  |  Issue : 1  |  Page : 12-19

Sensory brain responses and lateralization in nonpainful tactile stimuli during sleep


1 Department of Biophysics, Faculty of Medicine, Near East University, Mersin, Turkey
2 Department of Health Management, Faculty of Health Sciences, Near East University, Mersin, Turkey

Date of Submission28-Jun-2020
Date of Decision11-Aug-2020
Date of Acceptance20-Aug-2020
Date of Web Publication26-Mar-2021

Correspondence Address:
Gonca Inanc
Near East University, Near East Boulevard, 99138 Nicosia TRNC, Mersin 10
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/NSN.NSN_102_20

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  Abstract 


Aims and Objectives: The aim of this study was to investigate the difference between sensory brain responses of nonpainful tactile stimuli applied to the fingers of the right-hand dominant individuals between the hemispheres. Materials and Methods: Nineteen healthy volunteers (9 women, mean age ± standard deviation: 23.00 ± 2.24 years) participated in the study. Electroencephalogram (EEG) recordings were taken from 40 channels polysomnography system. A uniform nonpainful stimulus was applied to two fingers (index and middle fingers) of the right and left hand with a pneumatic stimulator unit. Results: Non-rapid eye movement sleep (NREM) whole night sleep-related potentials were evaluated. When the stimulus was applied to the right hand, central and parietal regions of the P50 response component appeared significantly earlier in the left hemisphere. When the left-hand stimulus was applied, the P50 and N100 response components appeared significantly early in central, parietal, and temporal regions in the left hemisphere. Hence, amplitudes of the right-hand response components (P50 and N100) were found to be greater in the central, parietal, and temporal regions in the left hemisphere. When the stimulus is applied to the left hand, the amplitude of the P50 component was greater in the central and temporal regions in the left hemisphere. Conclusion: P50 and N100 are components related to sensory processing. The difference in latency and amplitude observed in these components between hemispheres indicates the presence of lateralization in sensory processing during sleep.

Keywords: Electrophysiology, lateralization, sensory components, sleep


How to cite this article:
Inanc G, Özgören M, Öniz A. Sensory brain responses and lateralization in nonpainful tactile stimuli during sleep. Neurol Sci Neurophysiol 2021;38:12-9

How to cite this URL:
Inanc G, Özgören M, Öniz A. Sensory brain responses and lateralization in nonpainful tactile stimuli during sleep. Neurol Sci Neurophysiol [serial online] 2021 [cited 2021 Apr 16];38:12-9. Available from: http://www.nsnjournal.org/text.asp?2021/38/1/12/311961




  Introduction Top


Despite the fact that sleep research and clinical studies related to sleep disorders have substantially increased, the current science still carries a number of unknowns in the sleep domain. The former centuries even regarded sleep as a state between life and death. To this date, common knowledge dictates that wakefulness is an active but sleep is a passive state.

In a number of studies has been the advocates of the opposite view that sleep is an active state. Certainly, the cognitive prospect of the sleep is a curious one and currently a variety of properties of brain functioning during sleep is under scrutinization. Yet, the dynamic effects of the external stimulations on the brain during sleep - namely brain responsiveness - have not been fully uncovered.

One of the missing key components of sleep-related cognitive processing is the hemispheric attributions. The functional dominance of one hemisphere in relationship to a certain process is known as laterality.[1] The laterality concept has long been seen as a marker of brain's asymmetrical functionality. The initial neuroscientific clues have been historically provided by prominent works of Broca on aphasia patients. These studies have paved the way to concept of functional hemispheric dominance. Broca had provided the fact that the unilateral damage to one side of the brain - here the aphasia was related to left dominance - would alter the complex functions as there needed to be an asymmetry in the brain functionality.[2]

Historically, the concept of unilateral handedness had also been contributed to hemispheric dominance. The physical properties of both hands were similar, yet certain fine skills were attributed to one side only.[3] The Edinburgh questionnaire is commonly used to define general handedness; a negative laterality coefficient hence pointing left-hand dominance (and positive for the right hand).[4]

Consequently, the current study aims to highlight the hemispheric functional asymmetry against nonpainful tactile stimulations. To the best of our knowledge, this is the first study of its kind in processing specific somatosensory cognitive laterality during sleep.


  Subjects and Methods Top


This study was approved by the Institutional Ethics Evaluation Board (2011/16–16).

The study was conducted with 19 volunteers (9 females and 10 males; age range 23.00 ± 2.24 years).

Participants received necessary explanations about the study and their consents were obtained prior to recording. The hand preferences of the participants were determined with the “Edinburgh handedness inventory.” According to the Edinburgh handedness inventory, the laterality coefficient of the participants was calculated. Those with a negative laterality coefficient were evaluated as left handed and positive ones as right handed. The right hand was dominant in all participants.

Following the introductory remarks of the study design and procedures, the participants have filled a number of reports and scales. These include the State-Trait Anxiety Inventory (STAI) Form TX-1, the Symptom Checklist-90-Revised (SCL-90-R) tests, the Pittsburgh Sleep Quality Index, and Epworth Sleepiness Scale. None of the participants reported any psychiatric, neurologic, chronic illnesses as well as sleep disorders. In addition, the sleep behavior, coffee intake and/or other sleep altering conditions were reported.

The volunteers went through a first night sleep in an isolated room. The room was designed with a Faraday cage to minimize electric and electromagnetic noise and spikes. Furthermore, the acoustic isolation provided a conveniently quiet room. The room was dimly lit. An interactive audio system enabled communication when necessary. The entire session was video recorded with real-time stamps. The polysomnography recording was managed by NuAmps 40 channel (EEG, electrooculogram [EOG], and electromyogram [EMG]) system together with Embedded Microcontroller Stimulation Unit (EMISU),[5] pneumatic stimulation unit (Somatosensory Stimulus Generator 4-D Neuroimaging), and recording PC unit.

During EEG recording, the participants wore a fitting size Quick Cap (Neuromedical Supplies). The cap enabled a long-term comfortable whole head recording and the conductance was reassured with the electro gel (Electro-Gel, Electro-Cap International, Inc., US). EEG referencing was managed by interlinked ear lobe electrodes ([A1 + A2]/2).

The eye movements of the participants were monitored by electrodes placed at outer canthus of the right eye and left supraorbital areas. EMG activity was monitored by electrodes placed over supra and inferior chin areas. The overall electrode impedance was targeted to be kept lower than 5 kOhm and the continuous EEG recording sampling was maintained a 1 kHz sampling frequency. The nonpainful tactile stimulation was enabled by a pneumatic stimulation unit (4-D Neuroimaging Somatosensory Stimulus Generator).

The tactile stimulations were administered using a modified finger clip mechanism over index and mid fingers of right- and left-hand during sleep period. The modified finger clip mechanism incorporated a moving membrane with a contact area radius of 8–9 mm. This membrane was positioned to apply a soft pressure over fingertips. The pneumatic stimulation unit administered a certain amount of air on being triggered through in-house MATLAB stimulation system. This pressurized dry air puff action would mobilize the membrane thus resulting in a soft touch sensation on the participant's fingertips. In the study, nonpainful tactile evoked potential experiment design was used. In this design, a uniform pressure stimulus was used, and 30 stimuli were applied to one finger repeatedly, and 30 stimuli were applied to the other finger. This design was applied all night. The inter stimulus interval was around 3–3.5 s and the order of the stimulations had been randomized.

EEG evaluation was carried out as a post session after recording. The stages of sleep records were determined according to the AASM scoring system. The stimuli applied in the NREM stage were determined and the epochs were arranged as 1000 ms pre stimulus and 2000 ms poststimulus seeps. Out of these sweeps, the corresponding EOG channel was monitored and any amplitude exceeding ± 100 μV was eliminated. Furthermore, baseline correction and 0.5–30 Hz band pass filter (digital band filter with 12 dB/oct and zero phase shift, Neuroscan 4.5) were applied. Following these procedures, average files were formed for each sleep phase and each participant.

In the study, after the stimulus was applied, the time of occurrence of the response components was latency, and the voltage values of the response components were named as amplitude. In the measurement of the amplitudes of the electrophysiological responses, the largest amplitude responses between 0 and 2000 ms were measured in μV, and the time of occurrence of these responses was measured and evaluated in ms. The study consisted of NREM sleep stages.

The P50 response-component that occurred after the stimuli were applied-was 34–198 ms after the stimulus, the N100 response component was 60–274 ms after the stimulus. Accordingly, the P200 response was 140–350 ms after the stimulus, the N300 as 246–480 ms, the P450 as 388–592 ms, the N550 as 446–706 ms, the P900 as 620–954 ms, and the N_late response component was averaged as 868–1196 ms [Figure 1] poststimulus.
Figure 1: Average (N = 19) brain responses to nonpainful tactile stimulations in NREM sleep. The left panel indicates left hemisphere central (C3) responses whereas the right panel corresponds to C4 (right central region). The recordings are provided from central electrode sites on the scalp. The brain responses to right hand somatosensory stimulations are labeled as SEP-R (orange color) and hence the left as SEP-L (green color). The horizontal axis denotes time in ms, ranging from 1000 ms prestimulus to 2000 ms poststimulus (“-” value represents before the stimulus onset). The dashed vertical line represents the time point of stimulation. The vertical axis denotes amplitude (in μV, the reference marker points to the amplitude as in 2.5 μV scale) as positive values are given as the upper direction. In the left panel, appropriate labels are added in respective time windows as P50, N100, P200, N300, P450, N550, P900, and N_late. The P stands for positive and N for negative deflection

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In the current study, the latency and amplitudes of P50 and N100 response components, which are only the early sensory components, were primarily investigated.

In order to present and discuss the data in an uncomplicated manner, only 8 channel regions of interest that were prioritized over 40 EEG channels were examined as frontal, central, temporal, and parietal.

F3–F4, C3–C4, T3–T4, and P3–P4 electrodes were chosen primarily to compare the two hemispheres. In statistical analysis, Wilcoxon-signed rank test was used to compare the amplitude and latencies of the response components occurring in the left and right hemisphere of NREM sleep in SPSS 20 program (IBM Corp., New York, USA). P < 0.05 value was accepted for statistical significance. For the sake of simplicity only the early time window components, P50 and N100 are reported in this manuscript.


  Results Top


This study was comprised of recordings from whole night sleep in the sleep laboratory. The average sleep duration of all participants was found to be 7.5 h. The handedness laterality score of the participants was 82.58 ± 18.75 thus they were regarded as right-hand dominant. The current state of the subjects showed no signs of stress or psychiatric conditions, which was further approved by their STAI-TX1 and SCL-90R questionnaires. Primarily, 8 major regional electrodes (F3, F4, C3, C4, T3, T4, P3, P4) are reported [Figure 2]. Here, the right- and left-hand stimulations result in contralateral and ipsilateral responses.
Figure 2: Average (N = 19) brain responses to nonpainful tactile stimulations in NREM sleep. The recordings are provided from 8 major sites on the scalp (F: Frontal, C: Central, T: Temporal, and P: Parietal; even numbers right and odd numbers left hemisphere). The brain responses to right hand somatosensory stimulations are labeled as SEP-R (orange color) and hence the left as SEP-L (green color). The horizontal axis denotes time in ms, ranging from 1000 ms prestimulus to 2000 ms poststimulus (“-” value represents before the stimulus onset). The dashed vertical line represents the time point of stimulation. The vertical axis denotes amplitude (in μV, the reference marker points to the amplitude as in 2.5 μV scale) as positive values are given as the upper direction

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P50 component

Right-hand results

The P50 responses of the subjects during NREM sleep on nonpainful tactile stimulation of the right-hand index and middle fingers are provided as latency values and amplitudes [Table 1]. The table also displays the degree of hemispheric asymmetry and their corresponding P values (as in F3–F4, C3–C4, P3–P4, and T3–T4).
Table 1: The latency and amplitude of brain responses to left and right hand (index and middle fingers) somatosensory stimulations in 50 ms time window (labeled as P50) are provided for 19 subjects

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When the early onset (50 ms) of the brain responses derived from the right hand mid and index finger somatosensory stimulations were measured, the latency values were found to be earlier for left hemisphere (in central and parietal regions) than right hemisphere (ipsilateral) (respectively P = 0.037 and P = 0.013) [Table 1] and [Figure 3].
Figure 3: (a) The average latency of P50 responses to right hand stimulation during NREM sleep (N = 19). y-axis shows the latency of the P50 component in msec. (b) The average amplitude of P50 responses to right hand stimulation during NREM sleep (N = 19). y-axis shows the amplitude of the P50 component in μV. Light gray bars represent left hemisphere electrodes (F3, C3, P3, T3), whereas dark gray bars represent right hemisphere electrodes (F4, C4, P4, T4) (*P < 0.05, **P ≤ 0.01, ***P ≤ 0.001)

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The amplitude of the brain responses to right-hand somatosensory stimulation in P50 time window showed that the contralateral responses (hence left hemisphere) were larger than the ipsilateral ones in central, parietal, and temporal regions (P ≤ 0.001, P = 0.008, and P = 0.000, respectively) [Table 1] and [Figure 3].

Left-hand stimulation

The P50 responses of the subjects during NREM sleep on nonpainful tactile stimulation of the left-hand index and middle fingers are provided as latency values and amplitudes [Table 1].

The latency of the brain responses to left-hand somatosensory stimulation in P50 time window shows that the ipsilateral responses (hence left hemisphere) are earlier than the contralateral ones in central, parietal, and temporal regions (respectively, P = 0.031, P = 0.042 and P ≤ 0.001) [Table 1] and [Figure 4].
Figure 4: (a) The average latency of P50 responses to left-hand (N = 19) stimulation during NREM sleep. y-axis shows the latency of the P50 component in msec. (b) The average amplitude of P50 responses to left-hand stimulation during NREM sleep (N = 19). y-axis shows the amplitude of the P50 component in μV. Light gray bars represent left hemisphere electrodes (F3, C3, P3, T3), whereas dark gray bars represent right hemisphere electrodes (F4, C4, P4, T4), (*P < 0.05, **P ≤ 0.01, ***P ≤ 0.001)

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The amplitude of the brain responses to left-hand somatosensory stimulation in P50 time window shows that the contralateral responses (hence right hemisphere) are larger than the ipsilateral ones in central, and temporal regions (respectively, P ≤ 0.001, and P = 0.006) [Table 1] and [Figure 4].

N100 component

Right-hand results

The N100 responses of the subjects during NREM sleep on nonpainful tactile stimulation of the right-hand index and middle fingers are provided as latency values and amplitudes [Table 2].
Table 2: The latency and amplitude of brain responses to left and right hand (index and middle fingers) somatosensory stimulations in 100 ms time window (labeled as N100) are provided for 19 subjects

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When the early onset (100 ms) of the brain responses derived from the right hand mid and index finger somatosensory stimulations were measured, the latency values were not found to be significantly different for the left hemisphere (in central and parietal regions) than the right hemisphere (ipsilateral) [Table 2] and [Figure 5].
Figure 5: (a) The average latency of N100 responses to the right-hand stimulation during NREM sleep (N = 19). y-axis shows the latency of the N100 component in msec. (b) The average amplitude of N100 responses to right-hand stimulation during NREM sleep (N = 19). y-axis shows the amplitude of the N100 component in μV. Light gray bars represent left hemisphere electrodes (F3, C3, P3, T3), whereas dark gray bars represent right hemisphere electrodes (F4, C4, P4, T4), (**P ≤ 0.01, ***P ≤ 0.001)

Click here to view


The amplitude of the brain responses to right-hand somatosensory stimulation in N100 time window shows that the contralateral responses (hence left hemisphere) were larger than the ipsilateral ones in central, parietal, and temporal regions (respectively, P ≤ 0.001, P = 0.003 and P ≤ 0.001) [Table 2] and [Figure 5].

Left-hand results

The N100 responses of the subjects during NREM sleep on nonpainful tactile stimulation of the left-hand index and middle fingers are provided as latency values and amplitudes [Table 2].

The latency of the brain responses to left-hand somatosensory stimulation in N100 time window shows that the ipsilateral responses (hence left hemisphere) were earlier than the contralateral ones in central, parietal, and temporal regions (respectively, P = 0.008, P = 0.005 and P < 0.001) [Table 2] and [Figure 6]. The amplitude of the brain responses to left-hand somatosensory stimulation in N100 time window did not reveal significant difference between the contralateral responses (hence right hemisphere) and the ipsilateral ones in any region [Table 2] and [Figure 6].
Figure 6: (a) The average latency of N100 responses to left-hand stimulation during NREM sleep (N = 19). y-axis shows the latency of the P50 component in ms. (b) The average amplitude of N100 responses to left-hand stimulation during NREM sleep (N = 19). y-axis shows the amplitude of the N100 component in μV. Light gray bars represent left hemisphere electrodes (F3, C3, P3, T3), whereas dark gray bars represent right hemisphere electrodes (F4, C4, P4, T4), (**P ≤ 0.01, ***P ≤ 0.001)

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  Discussion Top


The whole night sleep recordings have provided early sensory (P50 and N100) brain responses to left- and right-hand stimulations.

Overall, the amplitudes of P50 and N100 components on right hand stimulation were found to be larger in left hemisphere (contralateral) than right hemisphere except for frontal regions. Additionally, P50 left-hand stimulation responses were larger in right hemisphere (contralateral) at central and temporal regions. As we know that P50 and N100 components are attributed to sensory processing.[6],[7] These results indicate that the cortical sensory processing continues in sleep. Furthermore, this cortical sensory processing has laterality (asymmetry between hemispheres).

When we compare the latencies (P50 component) on right hand stimulation, the left (contralateral) hemisphere (in central and parietal regions) reacted earlier. Conversely, the left-hand stimulation resulted in earlier left (ipsilateral) hemisphere latencies (P50 and N100) at central, temporal, and parietal regions.

Two explanations might be proposed in this context. First, as all the subjects were right-handed, we surely do not know yet how left-handed group would react. Thus, P50 and N100 latency differences might have risen from underlying hand (hemisphere) dominance. Second, regardless of hand dominance (and hence hemispheric dominance), the contralateral and ipsilateral latency variations might be highlighting the continuation of hemispheric asymmetry in sensory processing in sleep.

The functional background of the asymmetry (not only left and right but also posterior and frontal) in human brain is not completely understood. For instance, some papers addressed natural as well alertness processes as in the case of disturbing external conditions.[8],[9],[10],[11],[12],[13] Our study most probably is robust to disturbing conditions discussion as the stimulations were extremely soft and definitely pain free.

In some studies, it was shown that different regions of the brain go into sleep in different times, and while the frontal region goes into sleep the central regions follow later whereas the occipital region is still awake.[8] Furthermore, the EEG waveforms showed right hemisphere dominance at the early onset of the sleep.[9],[10],[11] Our study differs in the sense that the whole brain was evaluated across whole night NREM recordings. This should cancel out any possible confounding effect of different regions being in different stages at different times.

From experience, we all know that a sleeping person somehow is not fully isolated from the external world. In the literature, the level of responsiveness has been shown during sleep in the auditory modality.[14] The hemispheric asymmetry was shown with auditory stimulations in another study. Moreover, the observation of larger waveforms in one side was explained as the brain's effort of maintaining the sleep in that hemisphere.[15]

There are some behavioral studies addressing the onset of sleep in one hemisphere.[16] Under certain tasks, the reaction times of right or left hand during the transition from wakefulness to sleep were determined. It was concluded that left hemisphere shifted into sleep earlier than the right one. It was further indicated that the EEG waveforms and reaction times pointed the sleep onset different in two hemispheres.[17] Even though such studies may have focused on motor reactions rather than somatosensory, one may postulate that the motor and somatosensory processes are almost interwoven and alike.

In another study, the somatosensory potentials were evaluated (in a right-handed group) the dominant hemisphere presented larger potentials.[18] Likewise, Roth et al. showed that the left hemisphere was dominant in the right-handed participants.[12]

In the present study, we observed that both the right-hand (i.e., P50 and N100) and left-hand (i.e., P50) stimulations resulted in larger contralateral responses. Thus, we cannot follow the concept of different sleep onsets for different hemispheres point of view. Furthermore, our results are provided from whole night NREM sleep, which makes it impossible to favor a concept of time dependence. As these components are known to be related to sensory processing, we may conclude that the asymmetrical sensory processing continues. One may also feel the need to take out a similar design with left-handed participants.

Consequently, this study has brought insight to tactile sensory processing throughout the sleep as well as the related asymmetry of the brain. We also believe that our design might prove to be useful as a research setup for cognitive sensory processing of neurodegenerative and psychiatric disorders and their relationship to sleep. Furthermore, the sensory processing can shed some light into conditions like hemiplegia where different modalities are needed to be compared. Finally, as we are fast shifting into a world of brain computer interface, the understanding of the external stimulation, brain responsiveness and domain specify of the modalities may provide usefulness.

Acknowledgment

The authors would like to thank Serhat Taslica, R. Ugras Erdogan and Cagdas Guducu for technical support.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Sekimoto M, Kato M, Kajimura N, Watanabe T, Takahashi K, Okuma T. Asymmetric interhemispheric delta waves during all-night sleep in humans. Clin Neurophysiol 2000;111:924-8.  Back to cited text no. 13
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

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