Changes in sensory evoked responses coincide with rapid improvement in speech identification performance
TL;DR: Rapid physiological changes in the human auditory system that coincide with learning during a 1-hour test session in which participants learned to identify two consonant vowel syllables that differed in voice onset time are reported.
Abstract: Perceptual learning is sometimes characterized by rapid improvements in performance within the first hour of training (fast perceptual learning), which may be accompanied by changes in sensory and/or response pathways. Here, we report rapid physiological changes in the human auditory system that coincide with learning during a 1-hour test session in which participants learned to identify two consonant vowel syllables that differed in voice onset time. Within each block of trials, listeners were also presented with a broadband noise control stimulus to determine whether changes in auditory evoked potentials were specific to the trained speech cue. The ability to identify the speech sounds improved from the first to the fourth block of trials and remained relatively constant thereafter. This behavioral improvement coincided with a decrease in N1 and P2 amplitude, and these learning-related changes differed from those observed for the noise stimulus. These training-induced changes in sensory evoked responses were followed by an increased negative peak (between 275 and 330 msec) over fronto-central sites and by an increase in sustained activity over the parietal regions. Although the former was also observed for the noise stimulus, the latter was specific to the speech sounds. The results are consistent with a top-down nonspecific attention effect on neural activity during learning as well as a more learning-specific modulation, which is coincident with behavioral improvements in speech identification.
Citations
More filters
TL;DR: It is argued that despite exciting recent work on the role of neural synchronization in cognitive processes such as attention and perception, similar studies in the domain of learning and memory ––and priming, in particular––have been lacking.
Abstract: Stimulus repetition in identification tasks leads to improved behavioral performance (“repetition priming”) but attenuated neural responses (“repetition suppression”) throughout task-engaged cortical regions. While it is clear that this pervasive brain–behavior relationship reflects some form of improved processing efficiency, the exact form that it takes remains elusive. In this Discussion Paper, we review four different theoretical proposals that have the potential to link repetition suppression and priming, with a particular focus on a proposal that stimulus repetition affects improved efficiency throughenhanced neural synchronization. We argue that despite exciting recent work on the role of neural synchronization in cognitive processes such as attention and perception, similar studies in the domain of learning and memory ––and priming, in particular––have been lacking. We emphasize the need for new studies with adequate spatiotemporal resolution, formulate several novel predictions, and discuss our ongoing efforts to disentangle the current proposals.
189 citations
TL;DR: It is shown that subcortical and cortical neural plasticity interact to yield the linguistic advantages observed with musicianship, and infer that musicians have a refined hierarchy of internalized representations for auditory objects at both pre‐attentive and attentive levels that supplies more faithful phonemic templates to decision mechanisms governing linguistic operations.
Abstract: Musicianship is associated with neuroplastic changes in brainstem and cortical structures, as well as improved acuity for behaviorally relevant sounds including speech. However, further advance in the field depends on characterizing how neuroplastic changes in brainstem and cortical speech processing relate to one another and to speech-listening behaviors. Here, we show that subcortical and cortical neural plasticity interact to yield the linguistic advantages observed with musicianship. We compared brainstem and cortical neuroelectric responses elicited by a series of vowels that differed along a categorical speech continuum in amateur musicians and non-musicians. Musicians obtained steeper identification functions and classified speech sounds more rapidly than non-musicians. Behavioral advantages coincided with more robust and temporally coherent brainstem phase-locking to salient speech cues (voice pitch and formant information) coupled with increased amplitude in cortical-evoked responses, implying an overall enhancement in the nervous system's responsiveness to speech. Musicians' subcortical and cortical neural enhancements (but not behavioral measures) were correlated with their years of formal music training. Associations between multi-level neural responses were also stronger in musically trained listeners, and were better predictors of speech perception than in non-musicians. Results suggest that musicianship modulates speech representations at multiple tiers of the auditory pathway, and strengthens the correspondence of processing between subcortical and cortical areas to allow neural activity to carry more behaviorally relevant information. We infer that musicians have a refined hierarchy of internalized representations for auditory objects at both pre-attentive and attentive levels that supplies more faithful phonemic templates to decision mechanisms governing linguistic operations.
128 citations
Cites background from "Changes in sensory evoked responses..."
...…of the auditory ERPs (N1 and P2) are more sensitive to short- and long-term auditory training and speech signals than earlier components (Wood et al., 1971; Shahin et al., 2003; Alain et al., 2007; Alain et al., 2010; Ben-David et al., 2011; Sepp€anen et al., 2012; Bidelman et al., 2013b)....
[...]
...…to account for musicians’ behavioral speech and language benefits observed in this and a growing number of studies (e.g., Anvari et al., 2002; Chartrand & Belin, 2006; Slevc & Miyake, 2006; Bidelman & Krishnan, 2010; Zendel & Alain et al., 2010; Parbery-Clark et al., 2012; Strait et al., 2013)....
[...]
...Prior work has shown that of the obligatory ERPs, the N1 and P2 waves are the most sensitive to speech perception tasks (Wood et al., 1971; Alain et al., 2007, 2010; Ben-David et al., 2011; Bidelman et al., 2013b), and prone to the plastic effects of speech sound training (Tremblay et al., 2001;…...
[...]
...Increased cortical responses in the timeframe of N1-P2 have been observed with short-term speech training (Alain et al., 2007, 2010; Ben-David © 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of Neuroscience, 40, 2662–2673 et al., 2011), suggesting…...
[...]
TL;DR: The main finding was that the amplitude of the P1-N1-P2 auditory evoked response increased across repeated EEG sessions for all groups, regardless of any change in perceptual performance.
Abstract: Even though auditory training exercises for humans have been shown to improve certain perceptual skills of individuals with and without hearing loss, there is a lack of knowledge pertaining to which aspects of training are responsible for the perceptual gains, and which aspects of perception are changed. To better define how auditory training impacts brain and behavior, electroencephalography and magnetoencephalography have been used to determine the time course and coincidence of cortical modulations associated with different types of training. Here we focus on P1-N1-P2 auditory evoked responses (AEP), as there are consistent reports of gains in P2 amplitude following various types of auditory training experiences; including music and speech-sound training. The purpose of this experiment was to determine if the auditory evoked P2 response is a biomarker of learning. To do this, we taught native English speakers to identify a new pre-voiced temporal cue that is not used phonemically in the English language so that coinciding changes in evoked neural activity could be characterized. To differentiate possible effects of repeated stimulus exposure and a button-pushing task from learning itself, we examined modulations in brain activity in a group of participants who learned to identify the pre-voicing contrast and compared it to participants, matched in time, and stimulus exposure, that did not. The main finding was that the amplitude of the P2 auditory evoked response increased across repeated EEG sessions for all groups, regardless of any change in perceptual performance. What’s more, these effects were retained for months. Changes in P2 amplitude were attributed to changes in neural activity associated with the acquisition process and not the learned outcome itself. A further finding was the expression of a late negativity (LN) wave 600-900 ms post-stimulus onset, post-training, exclusively for the group that learned to identify the pre-voiced contrast.
119 citations
Cites background or methods from "Changes in sensory evoked responses..."
...This type of N1 behavior pattern is more in line with habituation and less so with the types of learning–related N1 changes exhibited during active EEG recordings where modulations in brain activity are recorded while the participant is attending and executing the training task (Alain et al., 2010)....
[...]
...In a series of past experiments, the effects of VOT training on the human P1-N1-P2 complex have also been studied (Tremblay et al., 2001, 2009, 2010; Sheehan et al., 2005; Alain et al., 2010)....
[...]
...To better define how auditory training exercises impact brain and behavior, electroencephalography (EEG) and magnetoencephalography (MEG) have been used to determine the time course and coincidence of cortical and sub-cortical modulations in evoked activity associated with different types of auditory training (Tremblay et al., 1997, 2001, 2009, 2010; Brattico et al., 2003; Shahin et al., 2003; Bosnyak et al., 2004; Sheehan et al., 2005; Alain et al., 2010; Carcagno and Plack, 2011; Shahin, 2011; Anderson et al., 2013; Barrett et al., 2013)....
[...]
...…activity associated with different types of auditory training (Tremblay et al., 1997, 2001, 2009, 2010; Brattico et al., 2003; Shahin et al., 2003; Bosnyak et al., 2004; Sheehan et al., 2005; Alain et al., 2010; Carcagno and Plack, 2011; Shahin, 2011; Anderson et al., 2013; Barrett et al., 2013)....
[...]
TL;DR: The results support a predictive coding account of speech perception; computational simulations show how a single mechanism, minimization of prediction error, can drive immediate perceptual effects of prior knowledge and longer-term perceptual learning of degraded speech.
Abstract: Human perception is shaped by past experience on multiple timescales. Sudden and dramatic changes in perception occur when prior knowledge or expectations match stimulus content. These immediate effects contrast with the longer-term, more gradual improvements that are characteristic of perceptual learning. Despite extensive investigation of these two experience-dependent phenomena, there is considerable debate about whether they result from common or dissociable neural mechanisms. Here we test single- and dual-mechanism accounts of experience-dependent changes in perception using concurrent magnetoencephalographic and EEG recordings of neural responses evoked by degraded speech. When speech clarity was enhanced by prior knowledge obtained from matching text, we observed reduced neural activity in a peri-auditory region of the superior temporal gyrus (STG). Critically, longer-term improvements in the accuracy of speech recognition following perceptual learning resulted in reduced activity in a nearly identical STG region. Moreover, short-term neural changes caused by prior knowledge and longer-term neural changes arising from perceptual learning were correlated across subjects with the magnitude of learning-induced changes in recognition accuracy. These experience-dependent effects on neural processing could be dissociated from the neural effect of hearing physically clearer speech, which similarly enhanced perception but increased rather than decreased STG responses. Hence, the observed neural effects of prior knowledge and perceptual learning cannot be attributed to epiphenomenal changes in listening effort that accompany enhanced perception. Instead, our results support a predictive coding account of speech perception; computational simulations show how a single mechanism, minimization of prediction error, can drive immediate perceptual effects of prior knowledge and longer-term perceptual learning of degraded speech.
108 citations
TL;DR: This review argues not only that common neural mechanisms for speech and music exist, but that experience in music leads to enhancements in sensory and cognitive contributors to speech processing, including reading and hearing speech in background noise.
Abstract: Human hearing depends on a combination of cognitive and sensory processes that function by means of an interactive circuitry of bottom-up and top-down neural pathways, extending from the cochlea to the cortex and back again. Given that similar neural pathways are recruited to process sounds related to both music and language, it is not surprising that the auditory expertise gained over years of consistent music practice fine-tunes the human auditory system in a comprehensive fashion, strengthening neurobiological and cognitive underpinnings of both music and speech processing. In this review we argue not only that common neural mechanisms for speech and music exist, but that experience in music leads to enhancements in sensory and cognitive contributors to speech processing. Of specific interest is the potential for music training to bolster neural mechanisms that undergird language-related skills, such as reading and hearing speech in background noise, which are critical to academic progress, emotional health, and vocational success.
100 citations
References
More filters
TL;DR: Auditory evoked potentials were recorded from the vertex of subjects who listened selectively to a series of tone pipping in one ear and ignored concurrent tone pips in the other ear to study the response set established to recognize infrequent, higher pitched tone pipped in the attended series.
Abstract: Auditory evoked potentials were recorded from the vertex of subjects who listened selectively to a series of tone pips in one ear and ignored concurrent tone pips in the other ear. The negative component of the evoked potential peaking at 80 to 110 milliseconds was substantially larger for the attended tones. This negative component indexed a stimulus set mode of selective attention toward the tone pips in one ear. A late positive component peaking at 250 to 400 milliseconds reflected the response set established to recognize infrequent, higher pitched tone pips in the attended series.
1,839 citations
"Changes in sensory evoked responses..." refers result in this paper
...This is consistent with findings showing that N1 amplitude is modulated by focused attention (Alain & Arnott, 2000; Hillyard, Hink, Schwent, & Picton, 1973 )....
[...]
TL;DR: The P300 wave is a positive deflection in the human event-related potential that may represent the transfer of information to consciousness, a process that involves many different regions of the brain.
Abstract: SummaryThe P300 wave is a positive deflection in the human event-related potential. It is most commonly elicited in an “oddball” paradigm when a subject detects an occasional “target” stimulus in a regular train of standard stimuli. The P300 wave only occurs if the subject is actively engaged in the
1,768 citations
"Changes in sensory evoked responses..." refers background in this paper
...Moreover, the P3b has been shown to increase in amplitude with increased stimulus discriminability (Mazaheri & Picton, 2005; Salisbury et al., 1994; Picton, 1992)....
[...]
...Moreover, the P3b has been shown to increase in amplitude with increased stimulus discriminability (Mazaheri & Picton, 2005; Salisbury et al., 1994; Picton, 1992)....
[...]
TL;DR: The results, when interpreted with evidence for modified somatosensory representations of the fingering digits in skilled violinists, suggest that use-dependent functional reorganization extends across the sensory cortices to reflect the pattern of sensory input processed by the subject during development of musical skill.
Abstract: Acoustic stimuli are processed throughout the auditory projection pathway, including the neocortex, by neurons that are aggregated into 'tonotopic' maps according to their specific frequency tunings. Research on animals has shown that tonotopic representations are not statically fixed in the adult organism but can reorganize after damage to the cochlea or after training the intact subject to discriminate between auditory stimuli. Here we used functional magnetic source imaging (single dipole model) to measure cortical representations in highly skilled musicians. Dipole moments for piano tones, but not for pure tones of similar fundamental frequency (matched in loudness), were found to be enlarged by about 25% in musicians compared with control subjects who had never played an instrument. Enlargement was correlated with the age at which musicians began to practise and did not differ between musicians with absolute or relative pitch. These results, when interpreted with evidence for modified somatosensory representations of the fingering digits in skilled violinists, suggest that use-dependent functional reorganization extends across the sensory cortices to reflect the pattern of sensory input processed by the subject during development of musical skill.
823 citations
"Changes in sensory evoked responses..." refers result in this paper
...A larger N1m, the magnetic counterpart of the electric N1, has also been found for piano tones compared with pure tones in musicians, whereas no such difference in brain response was found in nonmusicians (Pantev et al., 1998)....
[...]
TL;DR: Investigation of the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues found that attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape.
Abstract: We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.
787 citations
Additional excerpts
...discrimination learning (Fritz et al., 2003)....
[...]
TL;DR: It was concluded that the effect of selective auditory attention on the N1 component is not due solely to an enlargement of the exogenous N1 components of the vertex potential, but rather includes the addition of a prolonged endogenous component.
656 citations
"Changes in sensory evoked responses..." refers methods in this paper
...This may be similar to the processing negativity component used to account for the effects of attention on AEPs (Alain & Arnott, 2000; Alho,Tottola,Reinikainen,Sams,N Hansen & Hillyard, 1980 )....
[...]
...This may be similar to the processing negativity component used to account for the effects of attention on AEPs (Alain & Arnott, 2000; Alho, Tottola, Reinikainen, Sams,&Näätänen, 1987;Hansen & Hillyard, 1980)....
[...]