A striking feature of human perception is that our subjective experience depends not only on sensory information from the environment but also on our prior knowledge or expectations. The precise mechanisms by which sensory information and prior knowledge are integrated remain unclear, with longstanding disagreement concerning whether integration is strictly feedforward or whether higherlevel knowledge influences sensory processing through feedback connections. Here we used concurrent EEG and MEG recordings to determine how sensory information and prior knowledge are integrated in the brain during speech perception. We manipulated listeners' prior knowledge of speech content by presenting matching, mismatching, or neutral written text before a degraded (noise-vocoded) spoken word. When speech conformed to prior knowledge, subjective perceptual clarity was enhanced. This enhancement in clarity was associated with a spatiotemporal profile of brain activity uniquely consistent with a feedback process: activity in the inferior frontal gyrus was modulated by prior knowledge before activity in lower-level sensory regions of the superior temporal gyrus. In parallel, we parametrically varied the level of speech degradation, and therefore the amount of sensory detail, so that changes in neural responses attributable to sensory information and prior knowledge could be directly compared. Although sensory detail and prior knowledge both enhanced speech clarity, they had an opposite influence on the evoked response in the superior temporal gyrus. We argue that these data are best explained within the framework of predictive coding in which sensory activity is compared with top-down predictions and only unexplained activity propagated through the cortical hierarchy.
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 dualmechanism 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 learninginduced 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.perceptual learning | predictive coding | speech perception | magnetoencephalography | vocoded speech S uccessful perception in a dynamic and noisy environment critically depends on the brain's capacity to change how sensory input is processed based on past experience. Consider the way in which perception is enhanced by accurate prior knowledge or expectations. Sudden and dramatic changes in subjective experience can occur when a distorted and otherwise unrecognizable perceptual object is seen or heard after the object's identity is revealed (1-4). Such effects occur almost immediately; striking changes in perceptual outcomes occur over a timescale of seconds or less. However, not all effects of past experience emerge as rapidly as these effects of prior knowledge. With perceptual learning, practice in perceiving certain types of stimuli results in gradual and incremental improvements in perception that develop over a timescale of minutes or longer (Fig. 1A) (5, 6, 7). Critically, perceptual learning can generalize beyond the stimuli experienced during training, e.g., to visual forms presented in dif...
We use psychophysics and MEG to test how sensitivity to input statistics facilitates auditory-scene-analysis (ASA). Human subjects listened to ‘scenes’ comprised of concurrent tone-pip streams (sources). On occasional trials a new source appeared partway. Listeners were more accurate and quicker to detect source appearance in scenes comprised of temporally-regular (REG), rather than random (RAND), sources. MEG in passive listeners and those actively detecting appearance events revealed increased sustained activity in auditory and parietal cortex in REG relative to RAND scenes, emerging ~400 ms of scene-onset. Over and above this, appearance in REG scenes was associated with increased responses relative to RAND scenes. The effect of temporal structure on appearance-evoked responses was delayed when listeners were focused on the scenes relative to when listening passively, consistent with the notion that attention reduces ‘surprise’. Overall, the results implicate a mechanism that tracks predictability of multiple concurrent sources to facilitate active and passive ASA.DOI: http://dx.doi.org/10.7554/eLife.19113.001
Perception relies on the integration of sensory information and prior expectations. Here we show that selective neurodegeneration of human frontal speech regions results in delayed reconciliation of predictions in temporal cortex. These temporal regions were not atrophic, displayed normal evoked magnetic and electrical power, and preserved neural sensitivity to manipulations of sensory detail. Frontal neurodegeneration does not prevent the perceptual effects of contextual information; instead, prior expectations are applied inflexibly. The precision of predictions correlates with beta power, in line with theoretical models of the neural instantiation of predictive coding. Fronto-temporal interactions are enhanced while participants reconcile prior predictions with degraded sensory signals. Excessively precise predictions can explain several challenging phenomena in frontal aphasias, including agrammatism and subjective difficulties with speech perception. This work demonstrates that higher-level frontal mechanisms for cognitive and behavioural flexibility make a causal functional contribution to the hierarchical generative models underlying speech perception.
An unresolved question is how the reported clarity of degraded speech is enhanced when listeners have prior knowledge of speech content. One account of this phenomenon proposes top-down modulation of early acoustic processing by higher-level linguistic knowledge. Alternative, strictly bottom-up accounts argue that acoustic information and higher-level knowledge are combined at a late decision stage without modulating early acoustic processing. Here we tested top-down and bottom-up accounts using written text to manipulate listeners’ knowledge of speech content. The effect of written text on the reported clarity of noise-vocoded speech was most pronounced when text was presented before (rather than after) speech (Experiment 1). Fine-grained manipulation of the onset asynchrony between text and speech revealed that this effect declined when text was presented more than 120 ms after speech onset (Experiment 2). Finally, the influence of written text was found to arise from phonological (rather than lexical) correspondence between text and speech (Experiment 3). These results suggest that prior knowledge effects are time-limited by the duration of auditory echoic memory for degraded speech, consistent with top-down modulation of early acoustic processing by linguistic knowledge.
Semantically ambiguous words challenge speech comprehension, particularly when listeners must select a less frequent (subordinate) meaning at disambiguation. Using combined magnetoencephalography (MEG) and EEG, we measured neural responses associated with distinct cognitive operations during semantic ambiguity resolution in spoken sentences: (i) initial activation and selection of meanings in response to an ambiguous word and (ii) sentence reinterpretation in response to subsequent disambiguation to a subordinate meaning. Ambiguous words elicited an increased neural response approximately 400–800 msec after their acoustic offset compared with unambiguous control words in left frontotemporal MEG sensors, corresponding to sources in bilateral frontotemporal brain regions. This response may reflect increased demands on processes by which multiple alternative meanings are activated and maintained until later selection. Disambiguating words heard after an ambiguous word were associated with marginally increased neural activity over bilateral temporal MEG sensors and a central cluster of EEG electrodes, which localized to similar bilateral frontal and left temporal regions. This later neural response may reflect effortful semantic integration or elicitation of prediction errors that guide reinterpretation of previously selected word meanings. Across participants, the amplitude of the ambiguity response showed a marginal positive correlation with comprehension scores, suggesting that sentence comprehension benefits from additional processing around the time of an ambiguous word. Better comprehenders may have increased availability of subordinate meanings, perhaps due to higher quality lexical representations and reflected in a positive correlation between vocabulary size and comprehension success.
BackgroundThe time course and outcome of perceptual learning can be affected by the length and distribution of practice, but the training regimen parameters that govern these effects have received little systematic study in the auditory domain. We asked whether there was a minimum requirement on the number of trials within a training session for learning to occur, whether there was a maximum limit beyond which additional trials became ineffective, and whether multiple training sessions provided benefit over a single session.Methodology/Principal FindingsWe investigated the efficacy of different regimens that varied in the distribution of practice across training sessions and in the overall amount of practice received on a frequency discrimination task. While learning was relatively robust to variations in regimen, the group with the shortest training sessions (∼8 min) had significantly faster learning in early stages of training than groups with longer sessions. In later stages, the group with the longest training sessions (>1 hr) showed slower learning than the other groups, suggesting overtraining. Between-session improvements were inversely correlated with performance; they were largest at the start of training and reduced as training progressed. In a second experiment we found no additional longer-term improvement in performance, retention, or transfer of learning for a group that trained over 4 sessions (∼4 hr in total) relative to a group that trained for a single session (∼1 hr). However, the mechanisms of learning differed; the single-session group continued to improve in the days following cessation of training, whereas the multi-session group showed no further improvement once training had ceased.Conclusions/SignificanceShorter training sessions were advantageous because they allowed for more latent, between-session and post-training learning to emerge. These findings suggest that efficient regimens should use short training sessions, and optimized spacing between sessions.
Rhythmic sensory or electrical stimulation will produce rhythmic brain responses. These rhythmic responses are often interpreted as endogenous neural oscillations aligned (or “entrained”) to the stimulus rhythm. However, stimulus-aligned brain responses can also be explained as a sequence of evoked responses, which only appear regular due to the rhythmicity of the stimulus, without necessarily involving underlying neural oscillations. To distinguish evoked responses from true oscillatory activity, we tested whether rhythmic stimulation produces oscillatory responses which continue after the end of the stimulus. Such sustained effects provide evidence for true involvement of neural oscillations. In Experiment 1, we found that rhythmic intelligible, but not unintelligible speech produces oscillatory responses in magnetoencephalography (MEG) which outlast the stimulus at parietal sensors. In Experiment 2, we found that transcranial alternating current stimulation (tACS) leads to rhythmic fluctuations in speech perception outcomes after the end of electrical stimulation. We further report that the phase relation between electroencephalography (EEG) responses and rhythmic intelligible speech can predict the tACS phase that leads to most accurate speech perception. Together, we provide fundamental results for several lines of research—including neural entrainment and tACS—and reveal endogenous neural oscillations as a key underlying principle for speech perception.
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