Causal relationship between the right auditory cortex and speech-evoked envelope-following response: Evidence from combined transcranial stimulation and electroencephalography

Abstract

25Speech-evoked frequency-following response (FFR) reflects the neural encoding of speech 26 periodic information in the human auditory systems. FFR is of fundamental importance for 27 pitch and speech perception and serves as clinical biomarkers for various auditory and 28 language disorders. While it is suggested that the main neural source of FFR is in the auditory 29 brainstem, recent studies have shown a cortical contribution to FFR predominantly in the right 30 hemisphere. However, it is still unclear whether auditory cortex and FFR are causally related. 31The aim of this study was to establish this causal relationship using a combination of 32 transcranial direct current stimulation (tDCS) and scalp-recorded electroencephalography 33 (EEG). We applied tDCS over the left and right auditory cortices in right-handed normal-34 hearing participants and examined the after-effects of tDCS on FFR using EEG during 35 monaural listening to a repeatedly-presented speech syllable. Our results showed that: (1) 36 before tDCS was applied, participants had greater FFR magnitude when they listened to speech 37 from the left than the right ear, illustrating right-lateralized hemispheric asymmetry for FFR; 38(2) anodal and cathodal tDCS applied over the right, but not left, auditory cortex significantly 39 changed FFR magnitudes compared to the sham stimulation; specifically, such after-effects 40 occurred only when participants listened to speech from the left ear, emphasizing the right 41 auditory cortical contributions along the contralateral pathway. The current finding thus 42 provides the first causal evidence that validates the relationship between the right auditory 43 cortex and speech-evoked FFR and should significantly extend our understanding of speech 44 encoding in the brain. 45 46 Significance Statement 47 Speech-evoked frequency-following response (FFR) is a neural activity that reflects the brain's 48 encoding of speech periodic features. The FFR has great fundamental and clinical importance 49 for auditory processing. Whilst convention maintains that FFR derives mainly from the 50 brainstem, it has been argued recently that there are additional contributions to FFR from the 51 auditory cortex. Using a combination of tDCS, that altered neural excitability of auditory 52 cortices, and EEG recording, the present study provided the first evidence to validate a causal 53 relationship between the right auditory cortex and speech-evoked FFR. The finding supports 54 the right-asymmetric auditory cortical contributions to processing of speech periodicity and 55 3 advances our understanding of how speech signals are encoded and analysed along the central 56 auditory pathways. 57 58 82 White-Schwoch et al., 2015), dyslexia (Hornickel et al., 2013) and autism (Russo et al., 2008).83 It is argued that the fundamental and clinical importance of FFR is linked to the neural 84 fidelity of speech in the inferior colliculus at the brainstem, which has been proposed as the 85 4 main neural origin of FFR (Chandrasekaran and K...

Multiple Cases of Auditory Neuropathy Illuminate the Importance of Subcortical Neural Synchrony for Speech-in-noise Recognition and the Frequency-following Response

“…Our view may seem in tension with evidence that FFRs can ostensibly be recorded from auditory cortex. Such signals have been reported in healthy listeners using MEG (Coffey et al 2016), scalp EEG (Mai & Howell 2020), and intracranial EEG (Guo et al 2021). Our results predict these signals would be absent in listeners with neuropathy.…”