Generalization of sustained neurophysiological effects of short‐term auditory 13‐Hz stimulation to neighbouring frequency representation in humans

Abstract

A fuller understanding of the effects of auditory tetanization in humans would inform better language and sensory learning paradigms; however, there are still unanswered questions. Here, we probe sustained changes in the event‐related potentials (ERPs) to 1020‐ and 980‐Hz tones following a rapid presentation of 1020‐Hz tone (every 75 ms, 13.3 Hz, tetanization). Consistent with some previous studies, we revealed the increase in the P2 ERP component after tetanization. Contrary to some other studies, we did not observe the expected N1 increase after tetanization even in the identical experimental sequence. We detected a significant N1 decrease after tetanization. Expanding previous research, we showed that P2 increase and N1 decrease are not specific to the stimulus type (tetanized 1020 Hz and non‐tetanized 980 Hz), suggesting the generalizability of tetanization effect to the not‐stimulated auditory tones, at least to those of the neighbouring frequency. The ERPs' tetanization effects were observed for at least 30 min—the most prolonged interval examined, consistent with the duration of long‐term potentiation, LTP. In addition, the tetanization effects were detectable in the blocks where the participants watched muted videos, an experimental setting that can be easily used in children and other challenging groups. Thus, auditory 13‐Hz stimulation affects brain processing of tones including those of neighbouring frequencies.

Sensory Tetanization to Induce LTP-Like Plasticity: A Review and Reassessment of the Approach

“…Subsequent studies have since replicated these results in young healthy adults, reporting increases in the N1/N1b (and the C1, P1, P2) amplitude of sensory-evoked ERPs after tetanization (Kleeva et al, 2022; Lei et al, 2017; Lengali et al, 2021; McNair et al, 2006; Moore et al, 2020; Moore & Loprinzi, 2021; Normann et al, 2007; Ross et al, 2008; Rygvold et al, 2020; Smallwood et al, 2015; Spriggs et al, 2017; Spriggs et al, 2018; Spriggs et al, 2019; Sumner et al, 2018; Wilson et al, 2017; Zak et al, 2018). However, despite the number of studies finding sensory ERP amplitude increases after tetanization, several others have found no effect of tetanization on response amplitudes (D’Souza et al, 2018; Rygvold et al, 2020; Sumner et al, 2018) and several more have even found that response amplitudes decrease after tetanization (Kleeva et al, 2022; Klöppel et al, 2015; Rebreikina et al, 2021; Spriggs et al, 2018; Wynn et al, 2019). These contrasting effects of tetanization are also evident in fMRI studies, with three studies finding an increased BOLD response following tetanization (Clapp et al, 2005b; Wijtenburg et al, 2017; Zaehle et al, 2007) and one finding a decrease in BOLD response (Lahr et al, 2014).…”

“…The contrasting changes in sensory-evoked response amplitudes after sensory tetanization observed across studies suggests that sensory tetanization may not be a reliable tool for studying LTP-like plasticity. The same study design should not produce amplitude increases attributed to LTP in some studies (e.g., Kirk et al, 2021; Sanders et al, 2018; Sumner et al, 2020b) and amplitude decreases sometimes attributed to long- term depression (LTD, the opposite of LTP) in others (e.g., Abuleil et al, 2019; Kleeva et al, 2022). Any meaningful inference of the mechanisms that underlie changes in sensory-evoked response amplitudes after sensory tetanization are difficult given the contrasting effects reported across studies.…”

“…While sensory SENSORY TETANIZATION TO INDUCE LTP-LIKE PLASTICITY 24 tetanization may be a valuable non-invasive approach to induce LTP-like plasticity in humans (Kirk et al, 2021;Sumner et al, 2020b), contrasting effects across studies must be considered. As previously discussed, some studies find that tetanization can increase the amplitude of event related potentials (Kleeva et al, 2022;Lei et al, 2017;Lengali et al, 2021;McNair et al, 2006;Moore et al, 2020;Moore & Loprinzi, 2021;Normann et al, 2007;Ross et al, 2008;Rygvold et al, 2020;Smallwood et al, 2015;Spriggs et al, 2017;Spriggs et al, 2018;Spriggs et al, 2019;Sumner et al, 2018;Wilson et al, 2017;Zak et al, 2018), others find no change in response amplitude following tetanization (D'Souza et al, 2018;Rygvold et al, 2020;Sumner et al, 2018), and still others, including ourselves, find that response amplitudes decrease after tetanization (Kleeva et al, 2022;Klöppel et al, 2015;Rebreikina et al, 2021;Wynn et al, 2019). These conflicting results are troubling, especially when considering that most studies use methods very similar to those initially reported by Clapp et al (2005a) and Teyler et al (2005).…”

“…Auditory Tetanization. The auditory tetanization task was similar to procedures previously reported to elicit LTP-like changes in auditory ERP amplitudes (e.g., Clapp et al, 2005a;Kleeva et al, 2022). The stimuli used to elicit auditory ERPs were 1 kHz and 4 kHz tone-bursts with a duration of 50 ms (including a 5 ms ramp on and a 5 ms ramp off) presented at 90 dB SPL.…”

“…Similarly, tetanization to either the horizontal or vertical sine gradient similarly decreased the visual-evoked response amplitudes of both the horizontal and vertical sign gradients. Other studies have failed to find consistent stimulus-specific changes in sensory evoked responses after similar auditory tone-burst tetanization (Kleeva et al, 2022;Rebreikina et al, 2021) and visual sine-gradient tetanization (Cooke & Bear, 2010;Sumner et al, 2018). However, several other studies have found changes in sensory-evoked responses that are specific to the tetanized auditory toneburst (Kompus & Westerhausen, 2018;Mears & Spencer, 2012) and visual sinegradient (McNair et al, 2006;Ross et al, 2008;Spriggs et al, 2017;Wynn et al, 2019).…”