Neural coding of continuous speech in auditory cortex during monaural and dichotic listening

Abstract

The cortical representation of the acoustic features of continuous speech is the foundation of speech perception. In this study, noninvasive magnetoencephalography (MEG) recordings are obtained from human subjects actively listening to spoken narratives, in both simple and cocktail party-like auditory scenes. By modeling how acoustic features of speech are encoded in ongoing MEG activity as a spectrotemporal response function, we demonstrate that the slow temporal modulations of speech in a broad spectral region are represented bilaterally in auditory cortex by a phase-locked temporal code. For speech presented monaurally to either ear, this phase-locked response is always more faithful in the right hemisphere, but with a shorter latency in the hemisphere contralateral to the stimulated ear. When different spoken narratives are presented to each ear simultaneously (dichotic listening), the resulting cortical neural activity precisely encodes the acoustic features of both of the spoken narratives, but slightly weakened and delayed compared with the monaural response. Critically, the early sensory response to the attended speech is considerably stronger than that to the unattended speech, demonstrating top-down attentional gain control. This attentional gain is substantial even during the subjects' very first exposure to the speech mixture and therefore largely independent of knowledge of the speech content. Together, these findings characterize how the spectrotemporal features of speech are encoded in human auditory cortex and establish a single-trial-based paradigm to study the neural basis underlying the cocktail party phenomenon.

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

“…Auditory studies have similarly investigated the impact of pre-target oscillatory state but did so mostly in paradigms in which oscillations were driven by discrete and periodic stimuli. These auditory studies found effects mostly at lower frequencies, such as the delta and theta bands (Luo and Poeppel, 2007;Lakatos et al, 2009;Schroeder and Lakatos, 2009;Stefanics et al, 2010;Besle et al, 2011;Ding and Simon, 2012). Our results reiterate this importance of theta-band over alpha-band oscillations in auditory cortex for stimulus detection.…”

“…Previous work has shown that auditory entrainment prevails for oscillations Ͻ10 Hz (Luo and Poeppel, 2007;Kerlin et al, 2010;Ding and Simon, 2012;Ng et al, 2012). For our experimental setup, we found that centrally located auditory driven oscillations between 2 and 6 Hz exhibited the strongest entrainment as measured using the oscillatory ITC (see Materials and Methods and Fig.…”

“…The optimal frequency band for quantifying auditory-driven oscillations was determined as the frequency band exhibiting strongest entrainment (phase-locking) to natural sounds. Previous work has shown that entrainment of auditory oscillations derived from EEG, MEG, or intracortical data is strongest between 2 and 9 Hz (Luo and Poeppel, 2007;Kayser et al, 2009;Howard and Poeppel, 2010;Ding and Simon, 2012;Ng et al, 2012). For our experimental setup and natural sounds, we determined the optimal band using data acquired in a previous study (Ng et al, 2012), in which we presented a series of naturalistic sounds (a subset of those used to construct the background cacophony in the present study) for a prolonged period of time (52 s).…”

“…Histograms were aligned across subjects (aligned to bin 0). studies found reduced auditory entrainment in alpha compared with theta oscillations (Luo and Poeppel, 2007;Schroeder et al, 2008;Ding and Simon, 2012;Ng et al, 2012). Furthermore, although alpha signals may shape external attentional control on auditory cortex (Kerlin et al, 2010), the alpha rhythm of the auditory cortex itself does not seem crucial for the temporal hierarchy of oscillations implied in auditory scene analysis, which likely reflects the prominent timescales of natural sounds and speech (Ghitza, 2011).…”

“…Slow delta and theta oscillations entrain to sound sequences or speech, as evidenced by studies on humans (Luo and Poeppel, 2007;Howard and Poeppel, 2010;Ng et al, 2012;Pasley et al, 2012) or animals Kayser et al, 2009). One possibility by which entrainment can arise is that slow envelope modulations prominent in many natural sounds directly imprint on periodic excitability changes in cortical networks and effectively provide an intrinsic copy of the slow stimulus dynamics (Howard and Poeppel, 2010;Ding and Simon, 2012;Zion Golumbic et al, 2012). However, it could also well be that entrainment is induced by finer-grained (e.g., spectral) features of acoustic stimuli or higher-order properties of the temporal modulation spectrum, even in the absence of clearly visible envelope modulations (Ghitza, 2011).…”