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Abstract Vagus nerve stimulation (VNS) is being used increasingly to treat a wide array of diseases and disorders. This growth is driven in part by the putative ability to stimulate the nerve non-invasively. Despite decades of use and a rapidly expanding application space, we lack a complete understanding of the acute effects of VNS on human cortical neurophysiology. Here, we investigated cortical responses to sub-perceptual threshold cervical implanted (iVNS) and transcutaneous auricular (taVNS) vagus nerve stimulation using intracranial neurophysiological recordings in human epilepsy patients. To understand the areas that are modulated by VNS and how they differ depending on invasiveness and stimulation parameters, we compared VNS-evoked neural activity across a range of stimulation modalities, frequencies, and amplitudes. Using comparable stimulation parameters, both iVNS and taVNS caused subtle changes in low-frequency power across broad cortical networks, which were not the same across modalities and were highly variable across participants. However, within at least some individuals, it may be possible to elicit similar responses across modalities using distinct sets of stimulation parameters. These results demonstrate that both invasive and non-invasive VNS cause evoked changes in activity across a set of highly distributed cortical networks that are relevant to a diverse array of clinical, rehabilitative, and enhancement applications.

The human brain exhibits the remarkable ability to categorize speech sounds into distinct, meaningful percepts, even in challenging tasks like learning non-native speech categories in adulthood and hearing speech in noisy listening conditions. In these scenarios, there is substantial variability in perception and behavior, both across individual listeners and individual trials. While there has been extensive work characterizing stimulus-related and contextual factors that contribute to variability, recent advances in neuroscience are beginning to shed light on another potential source of variability that has not been explored in speech processing. Specifically, there are task-independent, moment-to-moment variations in neural activity in broadly-distributed cortical and subcortical networks that affect how a stimulus is perceived on a trial-by-trial basis. In this review, we discuss factors that affect speech sound learning and moment-to-moment variability in perception, particularly arousal states—neurotransmitter-dependent modulations of cortical activity. We propose that a more complete model of speech perception and learning should incorporate subcortically-mediated arousal states that alter behavior in ways that are distinct from, yet complementary to, top-down cognitive modulations. Finally, we discuss a novel neuromodulation technique, transcutaneous auricular vagus nerve stimulation (taVNS), which is particularly well-suited to investigating causal relationships between arousal mechanisms and performance in a variety of perceptual tasks. Together, these approaches provide novel testable hypotheses for explaining variability in classically challenging tasks, including non-native speech sound learning.

Adults struggle to learn non-native speech contrasts even after years of exposure. While laboratory-based training approaches yield learning, the optimal training conditions for maximizing speech learning in adulthood are currently unknown. Vagus nerve stimulation has been shown to prime adult sensory-perceptual systems towards plasticity in animal models. Precise temporal pairing with auditory stimuli can enhance auditory cortical representations with a high degree of specificity. Here, we examined whether sub-perceptual threshold transcutaneous vagus nerve stimulation (tVNS), paired with non-native speech sounds, enhances speech category learning in adults. Twenty-four native English-speakers were trained to identify non-native Mandarin tone categories. Across two groups, tVNS was paired with the tone categories that were easier- or harder-to-learn. A control group received no stimulation but followed an identical thresholding procedure as the intervention groups. We found that tVNS robustly enhanced speech category learning and retention of correct stimulus-response associations, but only when stimulation was paired with the easier-to-learn categories. This effect emerged rapidly, generalized to new exemplars, and was qualitatively different from the normal individual variability observed in hundreds of learners who have performed in the same task without stimulation. Electroencephalography recorded before and after training indicated no evidence of tVNS-induced changes in the sensory representation of auditory stimuli. These results suggest that paired-tVNS induces a temporally precise neuromodulatory signal that selectively enhances the perception and memory consolidation of perceptually salient categories.

In different tasks involving action perception, performance has been found to be facilitated when the presented stimuli were produced by the participants themselves rather than by another participant. These results suggest that the same mental representations are accessed during both production and perception. However, with regard to spoken word perception, evidence also suggests that listeners' representations for speech reflect the input from their surrounding linguistic community rather than their own idiosyncratic productions. Furthermore, speech perception is heavily influenced by indexical cues that may lead listeners to frame their interpretations of incoming speech signals with regard to speaker identity. In order to determine whether word recognition evinces similar self-advantages as found in action perception, it was necessary to eliminate indexical cues from the speech signal. We therefore asked participants to identify noise-vocoded versions of Dutch words that were based on either their own recordings or those of a statistically average speaker. The majority of participants were more accurate for the average speaker than for themselves, even after taking into account differences in intelligibility. These results suggest that the speech representations accessed during perception of noise-vocoded speech are more reflective of the input of the speech community, and hence that speech perception is not necessarily based on representations of one's own speech.