Sensitivity of offset and onset cortical auditory evoked potentials to signals in noise
Introduction
Successful perception of target auditory signals in a noisy or complex auditory scene depends on a number of factors, including the successful neural encoding of the signal in the auditory cortex. This encoding can be measured with scalp-recorded cortical auditory evoked potentials (CAEPs), a subset of electroencephalography (EEG) recordings, which can occur in response to both the onset and the offset of the stimulus. It has been suggested that the neural populations responsible for these two responses differ in important ways (Takahashi et al., 2004), and it is possible that they differ in their response to signals in noise. While the onset response has been used as a cortical measure of signal encoding in noise, the offset response has not. In this study we examine the effects of signal level and signal-to-noise ratio (SNR) on the offset response using two previously published onset datasets (Billings et al., 2007, Billings et al., 2009).
The extent to which the auditory evoked offset response differs from the auditory evoked onset response has been a central motivating question in the far-field study of offsets. Many of these studies have focused on shared physiological resources, and while many have suggested that the populations responsible for these two responses are the same or strongly overlapping (Hillyard and Picton, 1978, Hari et al., 1987, Joutsiniemi et al., 1989, Pantev et al., 1996), others have demonstrated significant differences (Noda et al., 1998, Wakai et al., 2007). Furthermore, near-field studies support the suggestion that different populations with different functional properties may be responsible for portions of the onset and offset responses. In general, onset units are far more prevalent than offset units and tend to be more tonotopically organized (Abeles and Goldstein, 1972, Phillips & Hall, 1990, He et al., 1997, Galazyuk and Feng, 1997, Recanzone, 2000, Phillips et al., 2002). It has been proposed that the offset response represents a rebound from inhibition, such that greater inhibition results in a larger offset response as inhibition is released (Henry, 1985, Henry and Lewis, 1988, Phillips et al., 2002, Takahashi et al., 2004). However, other studies have shown that offset responses can occur in the absence of onset-evoked inhibition, and have suggested that different sets of synaptic inputs are contributing to the different responses (Qin et al., 2007, Scholl et al., 2010).
A number of near-field studies examining the onset response have demonstrated robust sensitivity to SNR rather than absolute signal level when signals were presented in noise (Phillips, 1985, Phillips & Cynader, 1985, Phillips and Hall, 1986, Phillips & Kelly, 1992). Far-field evoked potential studies have investigated the effects of background noise on the onset response and have found similar effects, highlighting the encoding of SNR rather than absolute signal level when both cues are available (Burkard and Hecox, 1983, Burkard et al., 1997, Whiting et al., 1998, Kaplan-Neeman et al., 2006). Addressing this question directly, Billings et al. (2009) varied SNR for tonal stimuli at two different signal levels, and found that SNR and not absolute signal level had a significant effect on CAEP latency and amplitude. This sensitivity to SNR rather than signal level holds true for natural speech signals as well (Billings et al., in press). In quiet however, previous studies have demonstrated robust effects of signal level (Adler and Adler, 1989, Billings et al., 2007). Psychophysical studies have demonstrated effects of both SNR and absolute signal level for signals presented in noise (Hawkins and Stevens, 1950, Dirks et al., 1982, Studebaker et al., 1999, Hornsby et al., 2005). These findings suggest that absolute signal level is a behaviorally relevant cue even in the presence of background noise. It is therefore unclear why onsets do not appear to encode absolute signal level in noise. The goal of the present study was to determine whether the offset response shows a similar sensitivity to SNR and absolute signal level cues as the onset response.
Cortical auditory evoked potentials (CAEPs) were used to determine the effects of SNR and signal level on offset responses. Our goal was to analyze the offset response and compare it to the onset response in two previously published datasets (Billings et al., 2007, Billings et al., 2009), and to investigate the extent to which effects of SNR and signal level differ between the two responses.
Section snippets
Experimental conditions
Subject, stimulus, and recording procedures are described respectively in Billings et al. (2007) and Billings et al. (2009), and are summarized in Table 1. Briefly, Billings et al. (2007) presented 757 ms 1000-Hz pure tones (rise/fall time: 7.57 ms) at seven different intensity levels (30, 40, 50, 60, 70, 80, & 90 dB). Billings et al. (2009) used the same tone stimulus at two different signal levels (60 & 75 dB), but introduced continuous background noise at five different SNRs (20, 10, 0, −5, & −10
Results
Due to the large number of comparisons made in this study across individual waves (N1, P2, N2), electrode sites (Cz, GFP), and response type (onset, offset), Bonferroni corrections were applied across waves and electrode sites for each measure (peak latency, peak amplitude, and rectified area amplitude) independently, and p-values were modified accordingly. Also, since we used a statistical analysis that differed slightly from that reported in Billings et al., 2007, Billings et al., 2009, we
Discussion & conclusions
We set out to determine the effects of signal level and SNR on the CAEP offset response, and to compare these effects to previously published data on the CAEP onset response. Our results indicate that while both the onset and offset response provide evidence for the encoding of signal level in quiet and of SNR, only the offset response provides evidence for the encoding of signal level in the presence of noise.
Acknowledgements
We are grateful for helpful comments from Drs. Garnett McMillan, Erick Gallun, Melissa Papesh, and Tina Penman. This work is supported by the Department of Veterans Affairs through the Rehabilitation Research and Development Service with Career Development and Center of Excellence Grants (C6971M) and National Institutes of Health (NIDCD:DC010914).We are thankful to Kelly Tremblay and the Brain and Behavior Lab at the University of Washington where study design and collection of original data
References (37)
- et al.
Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs
Brain Res
(1972) - et al.
Human evoked cortical activity to signal-to-noise ratio and absolute signal level
Hear Res
(2009) - et al.
Modality-specificity of sensory aging in vision and audition: evidence from event-related potentials
Brain Res
(2008) Tuning of the auditory brainstem OFF responses is complementary to tuning of the auditory brainstem ON response
Hear Res
(1985)Temporal response features of cat auditory cortex neurons contributing to sensitivity to tones delivered in the presence of continuous noise
Hear Res
(1985)- et al.
Some neural mechanisms in the cat’s auditory cortex underlying sensitivity to combined tone and wide-spectrum noise stimuli
Hear Res
(1985) - et al.
Central auditory onset responses, and temporal asymmetries in auditory perception
Hear Res
(2002) Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys
Hear Res
(2000)- et al.
Nonoverlapping sets of synapses drive on responses and off responses in auditory cortex
Neuron
(2010) - et al.
On and Off magnetic auditory evoked responses in early infancy: a possible marker of brain immaturity
Clin Neurophysiol
(2007)
Influence of stimulus intensity on AEP components in the 80- to 200-millisecond latency range
Audiology
Lack of standard N2 in elderly participants indicates inhibitory processing deficit
Neuroreport
Effects of hearing aid amplification and stimulus intensity on cortical auditory evoked potentials
Audiol Neurootol
The effect of broadband noise on the human brainstem auditory evoked response. I. Rate and intensity effects
J Acoust Soc Am
The effects of click level, click rate, and level of background masking noise on the inferior colliculus potential (ICP) in the normal and the carboplatin-treated chinchilla
J Acoust Soc Am
Maturation of cortical sound processing as indexed by event-related potentials
Clin Neurophysiol
A procedure for quantifying the effects of noise on speech recognition
J Speech Hear Disord
Cited by (29)
Long-term training alters response dynamics in the aging auditory cortex
2024, Hearing ResearchOrbitofrontal cortex conveys stimulus and task information to the auditory cortex
2023, Current BiologyEffects of spatial separation with better- ear listening on N1–P2 complex
2021, Auris Nasus LarynxCitation Excerpt :Cortical responses differ in terms of the type of noise that will be present and the preferred SNR [16–19]. In literature, the use of different SNRs revealed varied effects of latencies and amplitudes on the N1–P2 complex [20–22]. Minimal or no effect on amplitude and latency was reported with high SNRs compared with low SNRs.
Early cortical processing of pitch height and the role of adaptation and musicality
2021, NeuroImageCitation Excerpt :Generally, sound offset plays an important role in auditory scene analysis (Bregman, 1990); nevertheless, offset responses have not received much attention, despite the fact that they appear in 30 - 70% of neurons in auditory cortex (for a review, see Kopp-Scheinpflug et al., 2018). Onset and offset responses have similar cortical generators (Pantev et al., 1996), and similar sensitivity to signal level, signal-to-noise ratio, and inter-stimulus interval (Takahashi et al., 2004; Yamashiro et al., 2009, 2011; Baltzell and Billings, 2014). More specifically, there is evidence that the timing of offset activity reflects the cessation of temporal regularity in the stimulus (Seither-Preisler et al., 2006; Krishnan et al., 2014), making it a form of pitch-related information in the offset response.
Event-related potential arithmetic to analyze offset potentials from conscious mice
2019, Journal of Neuroscience MethodsCitation Excerpt :Relatively low amplitudes of offset responses, and difficulty in isolating them, may explain why they have not previously been characterized in conscious rodent ERP studies. Additionally, the acoustic signal-to-noise ratio (SNR; >25 dB), between auditory stimuli and background noise, may have emphasized the offset response, given that on- and off-responses are sensitive to SNR (Baltzell and Billings, 2014). Previous studies in mice where the offset response was not present had SNRs of 5 dB (Maxwell et al., 2004) and 15 dB (Connolly et al., 2004).