The effect of vision on top.down modulation of hand blink reflex

Fatma Zehra Calikusu; Ayşegül Gündüz; Meral Kızıltan

doi:10.4103/NSN.NSN_77_20

ORIGINAL ARTICLE

Year : 2021 | Volume : 38 | Issue : 1 | Page : 6-11

The effect of vision on top.down modulation of hand blink reflex

Fatma Zehra Calikusu, Ayşegül Gündüz, Meral Kızıltan
Department of Neurology, Istanbul University-Cerrahpasa, Cerrahpasa Medical Faculty, Istanbul, Turkey

Date of Submission	26-Jun-2020
Date of Decision	11-Aug-2020
Date of Acceptance	12-Oct-2020
Date of Web Publication	26-Mar-2021

Correspondence Address:
Fatma Zehra Calikusu
Istanbul University Cerrahpasa, Cerrahpasa Medical Faculty Kocamustafapasa Street No: 53 Cerrahpasa 34098 Fatih, Istanbul
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/NSN.NSN_77_20

Abstract

Objective: The magnitude of hand blink reflex (HBR) increases when a threatening stimulus is positioned in the peripersonal space (PPS) compared with stimulus in the extrapersonal space (EPS). We hypothesized that the reflex increase in PPS might change depending on whether the stimulus was seen. We aimed to investigate the alterations in HBR response to understand the effects of vision on cortical modulation of HBR. Methods: The HBR was recorded from 11 healthy volunteers while the hand was far away from the face (EPS), close to the face with eyes open (PPS-eyes open), and close to the face with eyes closed (PPS-eyes closed). Changes in the response magnitudes were compared between the three conditions. Results: HBR was obtained in all subjects. As expected, there was an increase in the reflex magnitude in the PPS-eyes open condition relative to EPS. In the PPS-eyes closed condition, the duration and latency were shorter and the area under the curve was significantly smaller compared with the PPS-eyes open condition. Conclusion: The enhancement of HBR in PPS is attributed to tonic top-down modulation. Our study provides evidence for the special sensory modulation of the PPS effect on HBR and may suggest cortical modulation of top-down modulation of brainstem neural circuits.

Keywords: Hand-blink reflex, peripersonal space, vision

How to cite this article:
Calikusu FZ, Gündüz A, Kızıltan M. The effect of vision on top.down modulation of hand blink reflex. Neurol Sci Neurophysiol 2021;38:6-11

How to cite this URL:
Calikusu FZ, Gündüz A, Kızıltan M. The effect of vision on top.down modulation of hand blink reflex. Neurol Sci Neurophysiol [serial online] 2021 [cited 2023 Mar 28];38:6-11. Available from: http://www.nsnjournal.org/text.asp?2021/38/1/6/311971

Introduction

Hand blink reflex (HBR) or somatosensory blink reflex is the response on the orbicularis oculi muscle after the electrical stimulation of the median nerve.^[1],[2],[3] A subcortical circuit at the brainstem level creates this defensive reflex.^[1],[2],[3] In HBR, the response is bilateral with a latency of around 40–50 ms, which may correspond to the R2 component of the blink reflex obtained after the supraorbital electrical stimulation.^[1],[2],[3] The reflex magnitude in HBR increases when the stimulus approaches the face, or, in other words, when it is in the peripersonal space (PPS), which may be reduced by placing a screen between the face and the stimulus.^[4]

The HBR is enhanced as the stimulus producing it approaches the defensive PPS of the face, which has a protective function in primates as well as in humans.^[5] PPS neurons are found in the premotor region 6, parietal region (ventral intraparietal [VIP] region and Brodmann region 7b), and putamen.^[6],[7] The first detection of PPS was from single-unit electrophysiologic recording from visuotactile neurons of macaque monkeys. These neurons are sensitive to multiple sensory inputs, i.e., both visual and tactile stimuli, thus, the distance between the receptive field and the object is also important in the modulation of the stimulus.^[8]

Tactile neurons show somatotopic organization in the posterior parietal area, 7b inferior posterior, and VIP areas.^{[9],[10],[11],[12]} In particular, 85% of the tactile receptive area, which is stimulated from the monkey's neck, face, arm, hand, or both hands and face, is also sensitive to visual stimulation.^[10],[13] In facial and arm mapping, 33% of neurons are visuotactile.^{[9],[14],[15]} Crucially, subcortical regions also have a somatotopic arrangement similar to those in the parietal region, that is, these regions are in a close network with each other and there is intercommunication between them.^[11]

PPS is provided by processing and combining multiple senses.^[8] Sensory input, namely visual, tactile, and proprioceptive senses, are assembled to decide the last state of the motor system.^[16] The vision sense, in addition to the perception of space and moving objects, also plays a crucial role in proprioception, selective attention, and handling threatening stimuli.^[17],[18]

Taken together, although Sambo et al. suggested that vision had not an effect, we hypothesized that seeing the stimulus would change the response in defensive PPS.^[19]

Methods

Subjects

Eleven healthy volunteers (seven women; mean age ± standard deviation: 20.7 ± 2 years) with no history of neurologic disorders were enrolled in the study. Informed consent was obtained from all participants before enrollment in the study, which was approved by the local ethics committee in accordance with the tenets of the Declaration of Helsinki. Participants with a history of peripheral facial palsy and botulinum toxin or who had no HBR were excluded.

Electrophysiologic recordings

HBR was recorded from the left orbicularis oculi muscle in three different conditions: while the stimulated hand was in the extrapersonal space (EPS), in the PPS with eyes open (PPS-eyes open), and in the PPS with eyes closed (PPS-eyes closed) for each volunteer.

Participants were seated in a comfortable chair in the experiment room. Electrical stimuli were delivered using a surface bipolar electrode placed on the median nerve at the wrist. Electromyographic activity was recorded from the left orbicularis oculi muscle using pairs of surface electrodes with the active electrode over the mid-lower eyelid and the reference electrode a few centimeters laterally to the outer canthus. Electrophysiologic recordings were performed with Ag-AgCl surface electromyography recording electrodes using a Neuropack Σ-MEB-5504K measurement system (Nihon Kohden Corporation, Tokyo, Japan). Stimuli of 200 μs duration were delivered and stimulus intensity was increased until reproducible HBR (mean = 39.76 mA) was achieved. The recordings were analyzed using the settings of 30 ms/division and 200 or 500 μV/division.

We recorded in three different conditions, EPS, PPS-eyes open, and PPS-eyes closed. In the EPS condition, the participant's hand was freely placed on a pillow on the ipsilateral knee; the recording was taken when there was a distance of 50–60 cm. In the second step (PPS), the recording was made when the hand–eye distance was 3–4 cm. We assured that the hand did not touch the face. In the last step, the eyes were closed (PPS-eyes closed) without changing the position to investigate the effect of visual sensation. The eyes were covered with a piece of fabric to prevent the participant from seeing. This material was thick enough to prevent the light perception but was too thin to prevent the sense of the hand proximity. At this stage, participants were instructed to look across without closing their eyes. [Figure 1] shows these conditions. After reaching a reproducible HBR value for each participant, a total of 15 stimuli were given to the median nerve in three separate blocks. To prevent a habituation effect, a 30-s break was allowed between each stimulus. We recorded the HBR first in the EPS condition in each participant; however, PPS-eyes open and PPS-eyes closed conditions were randomized. Half of the participants received the PPS-eyes open condition first, and the other half received the PPS-eyes closed condition first with block randomization.

Figure 1: Illustration showing extrapersonal space (a), peripersonal space-eyes open (b), peripersonal space-eyes closed conditions (c)

Click here to view

Statistical analysis

In each block, reflex responses were rectified and averaged. We measured the onset latencies, duration, and peak-to-peak amplitudes of the HBR in each experiment. The area under the curve (AUC) of the HBR was calculated automatically offline.

The HBR latency, duration, amplitude, and AUC in each condition were compared. We first analyzed the normality of data. We used Friedman's test while comparing the reflex parameters between groups because the distribution was nonhomogenous. Comparisons were made between (1) EPS versus PPS-eyes open conditions; (2) PPS-eyes open versus PPS-eyes closed conditions; and (3) EPS versus PPS-eyes closed conditions using the Post hoc Wilcoxon signed-rank test (in-group analysis).

The statistical tests were conducted using the Statistical Package for the Social Sciences version 20 software (SPSS Inc., Chicago, IL, USA). P ≤ 0.050 were deemed statistically significant.

Results

The median values for EPS, PPS eyes closed, and PPS eyes open in latency were 55, 53, and 49, the median duration values were 39.6, 81, and 49.2, the median magnitude values were 28, 80, and 75, and the median AUC values were 0.5, 2.1, and 1.1, respectively.

A reproducible HBR was obtained by increasing the stimulus intensity in 11 participants with the mean amplitude of 69.8 ± 81.9 μV. The mean latency, duration, and AUC were 54.6 ± 4.4 ms, 56.4 ± 27.5 ms, and 0.9 ± 0.9 mV ms, respectively. [Table 1] shows detailed findings of HBR in three conditions.

Table 1: Hand blink reflex in three conditions

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Comparing EPS with PPS-eyes open, the amplitude, duration, and AUC values in PPS-eyes open condition were significantly greater than in the EPS condition (P-values: 0.005, 0.011, and 0.003, respectively) [Figure 2].

Figure 2: (a) The latency of hand blink reflex. (b) The duration of the hand blink reflex. (c) The area under the curve of the hand blink reflex. (d). The amplitude of hand blink reflex in extrapersonal space, peripersonal space-eyes open, and peripersonal space-eyes closed conditions. The latency of hand blink reflex was not statistically significantly different between peripersonal space-eyes open and extrapersonal space conditions, whereas it was significantly decreased in the peripersonal space-eye closed condition when compared with both extrapersonal space and peripersonal space-eye open conditions [Figure 2a]. The hand blink reflex duration was longer in PPS-eyes open than in extrapersonal space, but in the case of peripersonal space-eyes closed, it returned to values similar to those in extrapersonal space, i.e., as short as in extrapersonal space [Figure 2b]. The area under the curve was higher in the peripersonal space-eyes open condition than in the extrapersonal space condition, then it shrank in PPS-eyes closed but did not return to the state in extrapersonal space [Figure 2c]. There was no difference in amplitude between the peripersonal space-eyes open and peripersonal space-eyes closed conditions [Figure 2d]

Click here to view

Comparing EPS with PPS-eyes closed, the amplitude and AUC values in the PPS-eyes closed condition were significantly greater than in the EPS condition (P = 0.022, P = 0.021, respectively). The latency value in EPS was longer (P = 0.005) [Figure 2].

Comparing PPS-eyes open with PPS-eyes closed, the latency, duration, and AUC values in the PPS-eyes open condition were significantly greater than in the PPS-eyes closed condition (P-values: 0.013, 0.016, and 0.01, respectively) [Figure 2].

Discussion

The major findings were as follows (1) the onset latency in the PPS-eyes closed condition was even shorter than in the PPS-eyes open condition; (2) amplitude in PPS-eyes closed condition is smaller than PPS-eyes open but higher than in EPS; (3) duration in the PPS-eyes closed condition is shorter than in PPS-eyes open and similar to EPS; and (4) AUC in the PPS-eyes closed condition is smaller than in PPS-eyes open but higher than in EPS (possibly due to amplitude).

In this study, HBR responses from participants were recorded in three different situations: EPS, PPS-eyes open, and PPS-eyes closed. The effect of vision and proprioception on the reflex response in PPS and EPS was measured, and the HBR in PPS was compared with that of EPS. In the absence of vision in PPS in a healthy subject, we investigated whether the reflex response would preserve the expected enhancement as in PPS or would completely return to the status in EPS. The latency of a reflex stimulus reflects the conduction velocity in a circuit and the excitability of the circuit to some extent. The shortening of latency was shown in several studies covering the PPS-HBR association.^[19],[20] Although we were unable to show a similar shortening in the PPS-eyes open condition, significant shortening in the eyes closed condition suggests a clear effect of vision. Some previous studies also lacked the effect of PPS on R2 latency.^[19]

Behaviorally, shorter latencies suggest that the brain reacts more readily to stimuli when the eyes are closed. A previous study reported longer trigeminal blink reflex (TBR) latency by eyelid movement under normal conditions.^[21] Thus, the shorter latency after eye closure in our study may suggest the effect of visual pathways. We know that reflexes with generators in the brainstem are also under continuous control of suprasegmental structures other than PPS. For example, blink reflex after supraorbital trigeminal stimulation using electrical stimulus (TBR) or air-puff is modulated by attention to the supraorbital area.^{[22],[23],[24]} Inhibition of the visual cortex by repetitive transcranial magnetic stimulation created enhancement of nociceptive TBR suggesting a functional relation between the visual cortex and the trigeminal nociceptive system.^[25] Reducing the activity in visual pathways by eye closure decreases the time spent in the interneurons by the input before reaching the motoneurons. The shorter duration in the PPS-eye closure condition also supports the idea that the number of interneurons participating in the generation of the HBR is reduced under the effect of temporary vision loss.

Motor intention and planning, as well as proprioceptive inputs, have a crucial role in the increase in HBR magnitude.^[26] In recent studies, when vision and proprioceptive senses matched each other, continuous modulation in HBR was observed; however, in incongruent conditions, HBR modulation decreased.^[27] Top-down modulation in the brainstem might be attributed to the parietal area being informed by both proprioceptive inputs and vision.^[27] In this study, the enhancement of AUC values in the PPS-eyes closed condition compared with PPS-eyes open is evidence of reflex modulation of vision. In the PPS-eyes closed condition, AUC and amplitude values did not decrease as much as in the EPS condition, which can be interpreted as the continuation of the proprioception inputs on the reflex response.

Previously, the effect of vision on PPS was studied, and it was suggested that HBR did not change when the eye was closed, but our study provides clear evidence that it does change.^[28] The lack of a significant difference in PPS-eyes closed in previous studies may be due to the material used for covering the eye.^[4] A barrier, such as a screen, which creates a sense of physical distance, may also reduce the threatening effect of a stimulus. This reduction may be related to inhibition of proprioceptive stimulation by the screen. In our study, in contrast, we covered the eye with a thin material such as a piece of fabric so that only light perception and contrast were prevented, thus the stimulus still had a threatening effect. A more recent virtual reality study also confirmed the effect of vision on top-down modulation of HBR.^[27] However, a PPS representation similar to healthy subjects was defined in congenital blindness suggesting that subjects with persistent vision loss from childhood did not significantly affect the development of both one's own and others' PPS representation.^[29]

Performing EPS first in each participant may be considered a limitation of the study; however, the increase in the amplitude and AUC values in both PPS-eyes open and PPS-eyes closed conditions, in contrast to the expected decrease, indicates that there was no habituation effect. The reason for the lack of significant results might be attributed to the low number of participants.

Conclusion

The absence of vision does not lead to the total disappearance of the top-down modulation of HBR in the PPS. Therefore, proprioceptive inputs may play a more important role in shaping PPS than visual inputs. However, there is a clear effect of vision in PPS, and it may be interesting to study it in blind subjects to analyze the effect of long-term plastic changes in the visual cortex on PPS.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1.	Ellrich J, Bromm B, Hopf HC. Pain-evoked blink reflex. Muscle Nerve 1997;20:265-70.
2.	Cruccu G, Deuschl G. The clinical use of brainstem reflexes and hand-muscle reflexes. Clin Neurophysiol 2000;111:371-87.
3.	Miwa H, Nohara C, Hotta M, Shimo Y, Amemiya K. Somatosensory-evoked blink response: Investigation of the physiological mechanisms. Brain 1998;121(Pt 2):281-91.
4.	Sambo CF, Forster B, Williams SC, Iannetti GD. To blink or not to blink: Fine cognitive tuning of the defensive peripersonal space. J Neurosci 2012;32:12921-7.
5.	Somervail R, Bufacchi RJ, Guo Y, Kilintari M, Novembre G, Swapp D, et al. Movement of environmental threats modifies the relevance of the defensive eye-blink in a spatially-tuned manner. Sci Rep 2019;9:3661.
6.	Rizzolatti G, Fadiga L, Fogassi L, Gallese V. The space around us. Science 1997;277:190-1.
7.	Graziano MS. A system of multimodal areas in the primate brain. Neuron 2001;29:4-6.
8.	Fogassi L, Raos V, Franchi G, Gallese V, Luppino G, Matelli M. Visual responses in the dorsal premotor area F2 of the macaque monkey. Exp Brain Res 1999;128:194-9.
9.	Graziano MS, Gross CG. A bimodal map of space: Somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields. Exp Brain Res 1993;97:96-109.
10.	Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G. Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements. Exp Brain Res 1988;71:475-90.
11.	Leinonen L, Hyvärinen J, Nyman G, Linnankoski I. I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res 1979;34:299-320.
12.	Hyvärinen J, Shelepin Y. Distribution of visual and somatic functions in the parietal associative area 7 of the monkey. Brain Res 1979;169:561-4.
13.	Matelli M, Luppino G. Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 2001;14:S27-32.
14.	Leinonen L, Nyman G. II. Functional properties of cells in anterolateral part of area 7 associative face area of awake monkeys. Exp Brain Res 1979;34:321-33.
15.	Graziano MS, Gross CG. The representation of extrapersonal space: A possible role for bimodal, visual-tactile neurons. In: The cognitive neurosciences. Gazzaniga MS, editor. Cambridge, MA: MIT Press; 1994. p. 1021-34.
16.	Haggard P. Conscious intention and motor cognition. Trends Cogn Sci 2005;9:290-5.
17.	Wolpert DM, Ghahramani Z, Jordan MI. An internal model for sensorimotor integration. Science 1995;269:1880-2.
18.	Blakemore SJ, Wolpert DM, Frith CD. Abnormalities in the awareness of action. Trends Cogn Sci 2002;6:237-42.
19.	Sambo CF, Liang M, Cruccu G, Iannetti GD. Defensive peripersonal space: The blink reflex evoked by hand stimulation is increased when the hand is near the face. J Neurophysiol 2012;107:880-9.
20.	Sambo CF, Iannetti GD. Better safe than sorry? The safety margin surrounding the body is increased by anxiety. J Neurosci 2013;33:14225-30.
21.	Snow BJ, Frith RW. The relationship of eyelid movement to the blink reflex. J Neurol Sci 1989;91:179-89.
22.	de Tommaso M, Murasecco D, Libro G, Guido M, Sciruicchio V, Specchio LM, et al. Modulation of trigeminal reflex excitability in migraine: Effects of attention and habituation on the blink reflex. Int J Psychophysiol 2002;44:239-49.
23.	Schicatano EJ. The Effects of Attention on the Trigeminal Blink Reflex. Percept Mot Skills 2016;122:444-51.
24.	Hackley SA, Graham FK. Early selective attention effects on cutaneous and acoustic blink reflexes. Physiol Psychol 1983;11:235-42.
25.	Sava SL, de Pasqua V, Magis D, Schoenen J. Effects of visual cortex activation on the nociceptive blink reflex in healthy subjects. PLoS One 2014;9:e100198.
26.	Fossataro C, Bruno V, Gindri P, Garbarini F. Defending the body without sensing the body position: Physiological evidence in a brain-damaged patient with a proprioceptive deficit. Front Psychol 2018;9:2458.
27.	Fossataro C, Tieri G, Grollero D, Bruno V, Garbarini F. Hand blink reflex in virtual reality: The role of vision and proprioception in modulating defensive responses. Eur J Neurosci 2020;51:937-51.
28.	de Vignemont F, Iannetti GD. How many peripersonal spaces? Neuropsychologia 2015;70:327-34.
29.	Ricciardi E, Menicagli D, Leo A, Costantini M, Pietrini P, Sinigaglia C. Peripersonal space representation develops independently from visual experience. Sci Rep 2017;7:17673.