4.2 Response time reflects the mechanism of ephaptic coupling
Response times in our study are measured as the latency between the
onset of stimulation and the keypress from participants reporting seeing
a flash. Our findings reveal that multiple factors influence response
time, including stimulation polarity, amplitude modulation, and
intensity. Participants exhibited slower responses in cathodal otDCS
compared to tACS, in 2 Hz amplitude-modulated at 18 Hz compared to
sinusoidal at 18 Hz, and in threshold compared to suprathreshold
stimulations.
Among these findings, the effects of both intensity and AM can be
explained by the amount of delivered energy due to waveform shape and
amplitude. With the same peak-to-peak amplitude, AM stimulation could
deliver approximately half the energy of sinusoidal stimulation. In our
experiment, the threshold amplitude for AM stimulation is about 1.3
times that of sinusoidal stimulation, with the delivered energy being
approximately 65% of the threshold sinusoidal stimulation.
While the relationship between stimulation intensity and response time
is commonly observed in psychophysics studies, the underlying neural
mechanisms are rarely explained. Expanding on the global resonance
theory, our results can be elucidated by the occurrence of ephaptic
couplings in phosphene perception. Unlike typical synaptic transmission,
ephaptic coupling transfers information between adjacent neurons through
extracellular ion exchange or potential oscillation. It is thought to
influence the synchronization of neural spiking (Anastassiou et al.,
2011) and could be potent enough to elicit the firing of adjacent
pyramidal cells with a single action potential (Han et al., 2018).
Computational models propose that ephaptic coupling within neural
bundles may explain selective behavior (Chawla & Morgera, 2014),
responses to peripheral nerve stimulation (Capllonch-Juan & Sepulveda,
2020), and the propagation of epilepsy (Shivacharan et al., 2021). A
recent simulation study (Schmidt et al., 2021) demonstrated how ephaptic
couplings could contribute to response time. The model showed that
stronger stimulation triggers more neural spiking. While each spike
could induce ephaptic coupling within the neural bundle, collections of
ephaptic couplings become strong enough to elicit spiking volleys,
thereby increasing the velocity of neural transmission that leads to the
acceleration of response time. According to the model, not only are more
neural spiking elicited by stronger stimuli, but the stimulation effect
is also prolonged in the neural system.
This ephaptic coupling hypothesis could also explain the slower response
time in cathodal otDCS. It is possible that cathodal direct current
creates a hyper-polarized environment that makes it difficult to
maintain the spiking volley. Therefore, our response time results can be
explained by ephaptic coupling, which is considered the neural mechanism
of the global resonance theory.
Polarity effect may imply the selective effect of stimulation
One of the primary goals of our study is to examine the polarity effect
on phosphene perception. Compared to tACS, anodal otDCS induced brighter
phosphene, but no significant difference was found between cathodal
otDCS and tACS. However, cathodal otDCS did lead to longer response
times. Interestingly, none of the otDCS conditions influenced the
phosphene threshold, which is typically considered an index of neural
excitability. This result indicates that while the occurrence of
phosphenes is determined by electromagnetic oscillation, the perceptual
quality can be influenced by cortical excitability.
TES has been observed to influence visual perception in various ways. A
recent review discussed how noninvasive current stimulation over the
visual cortex can affect visual perception (Bello et al., 2023). It
suggested that anodal tDCS could marginally cause acute improvement in
contrast perception, and offline current stimulation (including both
tACS and anodal tDCS) could significantly enhance the ability of
contrast detection. However, this study did not find any tES effect on
response time, which contrasts our findings.
In a study that utilized the pedestal-delta-pedestal psychometric task
to explore the contrast detection function of different visual pathways
(Costa et al., 2015), a selective effect of tES was found. In the
4-alternate-forced-choice task, participants were asked to detect one of
the four squares that increased (inferred parvocellular pathway) or
decreased (inferred magnocellular pathway) its luminance in a different
amount from other squares for a short period. Their results showed that
during anodal tDCS, participants had a higher threshold for detecting
the target of decreasing luminance than sham stimulation, indicating
that anodal tDCS selectively affected the magnocellular pathway. The
magnocellular pathway is associated with the processing of motion,
depth, and high temporal and low spatial frequency information. In our
study, the impact of polarity on brightness perception might also
signify changes in the magnocellular pathway, as the perception of
phosphenes inherently indicates the detection of temporal contrast of
luminance.
Null result of intensity modulation on flash rate revealed
independence of AM information coding in phosphene percept
Our flash rate scoring revealed a significant effect in the AM
condition, consistent with our previous findings (Hsu et al., 2023).
Participants perceived the flash rate as slower under AM stimulation
than under sinusoidal stimulation. We observed a marginally significant
interaction between intensity and polarity (p = 0.07), indicating
that the flash rate was perceived faster under suprathreshold
stimulation only in the case of anodal AM otDCS (p = 0.01).
However, this effect was insignificant in other conditions, suggesting a
limited overall impact of intensity on flash rate scoring. In essence,
AM emerged as the primary determinant of the perceived flash rate,
implying that the AM frequency may be encoded by the perceptual system
and, at least partially, contribute to the perceived flash rate of
phosphene.
The current results, therefore, suggest the constitution of the AM
component in phosphene flash rate and provide strong evidence of
detecting the temporal envelope despite the spatial envelope in visual
perception.