The Associations of Hearing Sensitivity and Different Cognitive Functions with Perception of Speech-in-Noise.

OBJECTIVES: Impaired speech-in-noise perception affects individuals' daily lives and is a frequent symptom of age-related hearing loss, which is a common disabling condition and a health concern in aging populations. The relative impact of hearing sensitivity loss and different cognitive functions on speech-in-noise perception is not well understood. We aimed to assess to what extent hearing sensitivity and different cognitive functions were associated with sentence-in-noise performance across the adult lifespan. DESIGN: This study is based on data of 2585 participants of the Rhineland Study, which is a German community-based cohort study of persons of age 30 years and older. We assessed speech-in-noise with a sentence-in-noise test (Göttinger Satztest), hearing sensitivity thresholds (air conduction pure-tone audiometry [PTA] average of 0.5, 1, 2, and 4 kHz), and the following cognitive domains: crystallized intelligence (German Mehrfachwahl-Wortschatz-Intelligenztest, MWT-B), executive functioning (Trail Making Test B, TMT), working memory (Digit Span forward, DS), and long-term memory (Verbal Learning and Memory Test delayed recall; VLMT). We examined the association between hearing sensitivity and cognitive functions with sentence-in-noise perception using a multivariable linear regression model adjusted for age, sex, and multiple potential confounders. RESULTS: Better hearing sensitivity was associated with better speech-in-noise perception (0.25 signal noise ratio [SNR] dB HL decrease per 5 dB HL decrease in PTA; 95% confidence interval [CI]: 0.20 to 0.25; p < 0.001). Better cognitive performance was also associated with better speech-in-noise perception, but to a lesser extent. Crystallized intelligence (MWT-B) showed an effect size of -0.10 SNR dB HL decrease per SD (95% CI: -0.14 to -0.06; p < 0.001), executive functioning (TMT) of -0.08 SNR dB HL decrease per SD (95% CI: -0.13 to -0.03; p = 0.002), working memory (DS) of -0.04 SNR dB HL decrease per SD (95% CI: -0.08 to -0.003; p = 0.03), and long-term memory (VLMT) of -0.03 SNR dB HL decrease per SD (95% CI: -0.07 to 0.01; p = 0.12). The standardized effect of hearing sensitivity (ß = 0.34) on speech-in-noise perception was four to five times larger than the effects of crystallized intelligence (ß = -0.08) and executive functioning (ß = -0.06). CONCLUSIONS: Hearing sensitivity was the strongest determinant of sentence-in-noise perception in adults above the age of 30. We determined the relative effect of different cognitive functions on sentence-in-noise perception. Crystallized intelligence and executive functions showed stronger associations while working and long-term memory functions had much smaller independent effects. Our results contribute to the understanding of determinants of speech-in-noise perception in aging adults.

A Functional MRI Paradigm for Efficient Mapping of Memory Encoding Across Sensory Conditions.

We introduce a new and time-efficient memory-encoding paradigm for functional magnetic resonance imaging (fMRI). This paradigm is optimized for mapping multiple contrasts using a mixed design, using auditory (environmental/vocal) and visual (scene/face) stimuli. We demonstrate that the paradigm evokes robust neuronal activity in typical sensory and memory networks. We were able to detect auditory and visual sensory-specific encoding activities in auditory and visual cortices. Also, we detected stimulus-selective activation in environmental-, voice-, scene-, and face-selective brain regions (parahippocampal place and fusiform face area). A subsequent recognition task allowed the detection of sensory-specific encoding success activity (ESA) in both auditory and visual cortices, as well as sensory-unspecific positive ESA in the hippocampus. Further, sensory-unspecific negative ESA was observed in the precuneus. Among others, the parallel mixed design enabled sustained and transient activity comparison in contrast to rest blocks. Sustained and transient activations showed great overlap in most sensory brain regions, whereas several regions, typically associated with the default-mode network, showed transient rather than sustained deactivation. We also show that the use of a parallel mixed model had relatively little influence on positive or negative ESA. Together, these results demonstrate a feasible, versatile, and brief memory-encoding task, which includes multiple sensory stimuli to guarantee a comprehensive measurement. This task is especially suitable for large-scale clinical or population studies, which aim to test task-evoked sensory-specific and sensory-unspecific memory-encoding performance as well as broad sensory activity across the life span within a very limited time frame.

Previous Musical Experience and Cortical Thickness Relate to the Beneficial Effect of Motor Synchronization on Auditory Function.

Auditory processing can be enhanced by motor system activity. During auditory-motor synchronization, motor activity guides auditory attention and thus facilitates auditory processing through active sensing. Previous research on enhanced auditory processing through motor synchronization has been limited to easy tasks with simple stimulus material. Further, the mechanisms and brain regions underlying this synchronization are unclear. We investigated the effect of motor synchronization on auditory processing with naturalistic, musical auditory material in a discrimination task. We further assessed how previous musical training and cortical thickness of specific brain regions relate to different aspects of auditory-motor synchronization. We conducted an auditory-motor experiment in 139 adults. The task involved melody discrimination and beat tapping synchronization. Additionally, 68 participants underwent structural MRI. We found that individuals with better auditory-motor synchronization accuracy showed improved melody discrimination, and that melody discrimination was better in trials with higher tapping accuracy. However, melody discrimination was worse in the tapping than in the listening only condition. Longer previous musical training and thicker Heschl's gyri were associated with better melody discrimination and better tapping synchrony. Post hoc analyses furthermore pointed to a possible moderating role of frontal regions. Our results suggest that motor synchronization can enhance auditory discrimination abilities through active sensing, but that this beneficial effect can be counteracted by dual-task inference when the two tasks are too challenging. Moreover, prior experience and structural brain differences influence the extent to which an individual can benefit from motor synchronization in complex listening. This could inform future research directed at development of personalized training programs for hearing ability.

Neural Correlates of Early Sound Encoding and their Relationship to Speech-in-Noise Perception.

Speech-in-noise (SIN) perception is a complex cognitive skill that affects social, vocational, and educational activities. Poor SIN ability particularly affects young and elderly populations, yet varies considerably even among healthy young adults with normal hearing. Although SIN skills are known to be influenced by top-down processes that can selectively enhance lower-level sound representations, the complementary role of feed-forward mechanisms and their relationship to musical training is poorly understood. Using a paradigm that minimizes the main top-down factors that have been implicated in SIN performance such as working memory, we aimed to better understand how robust encoding of periodicity in the auditory system (as measured by the frequency-following response) contributes to SIN perception. Using magnetoencephalograpy, we found that the strength of encoding at the fundamental frequency in the brainstem, thalamus, and cortex is correlated with SIN accuracy. The amplitude of the slower cortical P2 wave was previously also shown to be related to SIN accuracy and FFR strength; we use MEG source localization to show that the P2 wave originates in a temporal region anterior to that of the cortical FFR. We also confirm that the observed enhancements were related to the extent and timing of musicianship. These results are consistent with the hypothesis that basic feed-forward sound encoding affects SIN perception by providing better information to later processing stages, and that modifying this process may be one mechanism through which musical training might enhance the auditory networks that subserve both musical and language functions.

Cortical contributions to the auditory frequency-following response revealed by MEG.

The auditory frequency-following response (FFR) to complex periodic sounds is used to study the subcortical auditory system, and has been proposed as a biomarker for disorders that feature abnormal sound processing. Despite its value in fundamental and clinical research, the neural origins of the FFR are unclear. Using magnetoencephalography, we observe a strong, right-asymmetric contribution to the FFR from the human auditory cortex at the fundamental frequency of the stimulus, in addition to signal from cochlear nucleus, inferior colliculus and medial geniculate. This finding is highly relevant for our understanding of plasticity and pathology in the auditory system, as well as higher-level cognition such as speech and music processing. It suggests that previous interpretations of the FFR may need re-examination using methods that allow for source separation.

Song Perception by Professional Singers and Actors: An MEG Study.

The cortical correlates of speech and music perception are essentially overlapping, and the specific effects of different types of training on these networks remain unknown. We compared two groups of vocally trained professionals for music and speech, singers and actors, using recited and sung rhyme sequences from German art songs with semantic and/ or prosodic/melodic violations (i.e. violations of pitch) of the last word, in order to measure the evoked activation in a magnetoencephalographic (MEG) experiment. MEG data confirmed the existence of intertwined networks for the sung and spoken modality in an early time window after word violation. In essence for this early response, higher activity was measured after melodic/prosodic than semantic violations in predominantly right temporal areas. For singers as well as for actors, modality-specific effects were evident in predominantly left-temporal lateralized activity after semantic expectancy violations in the spoken modality, and right-dominant temporal activity in response to melodic violations in the sung modality. As an indication of a special group-dependent audiation process, higher neuronal activity for singers appeared in a late time window in right temporal and left parietal areas, both after the recited and the sung sequences.

Dissociation of Neural Networks for Predisposition and for Training-Related Plasticity in Auditory-Motor Learning.

Skill learning results in changes to brain function, but at the same time individuals strongly differ in their abilities to learn specific skills. Using a 6-week piano-training protocol and pre- and post-fMRI of melody perception and imagery in adults, we dissociate learning-related patterns of neural activity from pre-training activity that predicts learning rates. Fronto-parietal and cerebellar areas related to storage of newly learned auditory-motor associations increased their response following training; in contrast, pre-training activity in areas related to stimulus encoding and motor control, including right auditory cortex, hippocampus, and caudate nuclei, was predictive of subsequent learning rate. We discuss the implications of these results for models of perceptual and of motor learning. These findings highlight the importance of considering individual predisposition in plasticity research and applications.

Clinical investigations of receptive and expressive musical functions after stroke.

There is a long tradition of investigating various disorders of musical abilities after stroke. These impairments, associated with acquired amusia, can be highly selective, affecting only music perception (i.e., receptive abilities/functions) or expression (music production abilities), and some patients report that these may dramatically influence their emotional state. The aim of this study was to systematically test both the melodic and rhythmic domains of music perception and expression in left- and right-sided stroke patients compared to healthy subjects. Music perception was assessed using rhythmic and melodic discrimination tasks, while tests of expressive function involved the vocal or instrumental reproduction of rhythms and melodies. Our approach revealed deficits in receptive and expressive functions in stroke patients, mediated by musical expertise. Those patients who had experienced a short period of musical training in childhood and adolescence performed better in the receptive and expressive subtests compared to those without any previous musical training. While discrimination of specific musical patterns was unimpaired after a left-sided stroke, patients with a right-sided stroke had worse results for fine melodic and rhythmic analysis. In terms of expressive testing, the most consistent results were obtained from a test that required patients to reproduce sung melodies. This implies that the means of investigating production abilities can impact the identification of deficits.

Musical expertise is related to neuroplastic changes of multisensory nature within the auditory cortex.

Recent neuroscientific evidence indicates that multisensory integration does not only occur in higher level association areas of the cortex as the hierarchical models of sensory perception assumed, but also in regions traditionally thought of as unisensory, such as the auditory cortex. Nevertheless, it is not known whether expertise-induced neuroplasticity can alter the multisensory processing that occurs in these low-level regions. The present study used magnetoencephalography to investigate whether musical training may induce neuroplastic changes of multisensory processing within the human auditory cortex. Magnetoencephalography data of four different experiments were used to demonstrate the effect of long-term and short-term musical training on the integration of auditory, somatosensory and visual stimuli in the auditory cortex. The cross-sectional design of three of the experiments allowed us to infer that long-term musical training is related to a significantly different way of processing multisensory information within the auditory cortex, whereas the short-term training design of the fourth experiment allowed us to causally infer that multisensory music reading training affects the multimodal processing within the auditory cortex.

Tones and numbers: a combined EEG-MEG study on the effects of musical expertise in magnitude comparisons of audiovisual stimuli.

This study investigated the cortical responses underlying magnitude comparisons of multisensory stimuli and examined the effect that musical expertise has in this process. The comparative judgments were based on a newly learned rule binding the auditory and visual stimuli within the context of magnitude comparisons: "the higher the pitch of the tone, the larger the number presented." The cortical responses were measured by simultaneous MEG\EEG recordings and a combined source analysis with individualized realistic head models was performed. Musical expertise effects were investigated by comparing musicians to non-musicians. Congruent audiovisual stimuli, corresponding to the newly learned rule, elicited activity in frontotemporal and occipital areas. In contrast, incongruent stimuli activated temporal and parietal regions. Musicians when compared with nonmusicians showed increased differences between congruent and incongruent stimuli in a prefrontal region, thereby indicating that music expertise may affect multisensory comparative judgments within a generalized representation of analog magnitude.

Temporal processing of audiovisual stimuli is enhanced in musicians: evidence from magnetoencephalography (MEG).

Numerous studies have demonstrated that the structural and functional differences between professional musicians and non-musicians are not only found within a single modality, but also with regard to multisensory integration. In this study we have combined psychophysical with neurophysiological measurements investigating the processing of non-musical, synchronous or various levels of asynchronous audiovisual events. We hypothesize that long-term multisensory experience alters temporal audiovisual processing already at a non-musical stage. Behaviorally, musicians scored significantly better than non-musicians in judging whether the auditory and visual stimuli were synchronous or asynchronous. At the neural level, the statistical analysis for the audiovisual asynchronous response revealed three clusters of activations including the ACC and the SFG and two bilaterally located activations in IFG and STG in both groups. Musicians, in comparison to the non-musicians, responded to synchronous audiovisual events with enhanced neuronal activity in a broad left posterior temporal region that covers the STG, the insula and the Postcentral Gyrus. Musicians also showed significantly greater activation in the left Cerebellum, when confronted with an audiovisual asynchrony. Taken together, our MEG results form a strong indication that long-term musical training alters the basic audiovisual temporal processing already in an early stage (direct after the auditory N1 wave), while the psychophysical results indicate that musical training may also provide behavioral benefits in the accuracy of the estimates regarding the timing of audiovisual events.

Multisensory integration during short-term music reading training enhances both uni- and multisensory cortical processing.

The human ability to integrate the input of several sensory systems is essential for building a meaningful interpretation out of the complexity of the environment. Training studies have shown that the involvement of multiple senses during training enhances neuroplasticity, but it is not clear to what extent integration of the senses during training is required for the observed effects. This study intended to elucidate the differential contributions of uni- and multisensory elements of music reading training in the resulting plasticity of abstract audiovisual incongruency identification. We used magnetoencephalography to measure the pre- and posttraining cortical responses of two randomly assigned groups of participants that followed either an audiovisual music reading training that required multisensory integration (AV-Int group) or a unisensory training that had separate auditory and visual elements (AV-Sep group). Results revealed a network of frontal generators for the abstract audiovisual incongruency response, confirming previous findings, and indicated the central role of anterior prefrontal cortex in this process. Differential neuroplastic effects of the two types of training in frontal and temporal regions point to the crucial role of multisensory integration occurring during training. Moreover, a comparison of the posttraining cortical responses of both groups to a group of musicians that were tested using the same paradigm revealed that long-term music training leads to significantly greater responses than the short-term training of the AV-Int group in anterior prefrontal regions as well as to significantly greater responses than both short-term training protocols in the left superior temporal gyrus (STG).

Audio-tactile integration and the influence of musical training.

Perception of our environment is a multisensory experience; information from different sensory systems like the auditory, visual and tactile is constantly integrated. Complex tasks that require high temporal and spatial precision of multisensory integration put strong demands on the underlying networks but it is largely unknown how task experience shapes multisensory processing. Long-term musical training is an excellent model for brain plasticity because it shapes the human brain at functional and structural levels, affecting a network of brain areas. In the present study we used magnetoencephalography (MEG) to investigate how audio-tactile perception is integrated in the human brain and if musicians show enhancement of the corresponding activation compared to non-musicians. Using a paradigm that allowed the investigation of combined and separate auditory and tactile processing, we found a multisensory incongruency response, generated in frontal, cingulate and cerebellar regions, an auditory mismatch response generated mainly in the auditory cortex and a tactile mismatch response generated in frontal and cerebellar regions. The influence of musical training was seen in the audio-tactile as well as in the auditory condition, indicating enhanced higher-order processing in musicians, while the sources of the tactile MMN were not influenced by long-term musical training. Consistent with the predictive coding model, more basic, bottom-up sensory processing was relatively stable and less affected by expertise, whereas areas for top-down models of multisensory expectancies were modulated by training.

Non-pharmacological interventions and neuroplasticity in early stage Alzheimer's disease.

Non-pharmacological interventions have the potential to reduce cognitive decline and to improve psychosocial aspects in mild cognitive impairment and Alzheimer's dementia, and the absence of side effects makes them a favorable option also for preventive strategies. We provide an overview on recent studies involving cognitive training and reminiscence, stimulating and challenging experiences such as visual art and music, physical activities, and electromagnetic stimulation. We review findings on neuroplasticity in the aging brain and their relevance for cognitive improvement in patients with neurodegenerative diseases. We discuss cognitive reserve and possible mechanisms that drive neuroplasticity and new learning. Finally, we identify promising avenues for future intervention strategies and research, such as combinations of cognitive and pharmaceutical interventions, and individual strategies adapted to the disease stage and tailored to the needs, predispositions and preferences of patients.

Task decomposition: a framework for comparing diverse training models in human brain plasticity studies.

Training studies, in which the structural or functional neurophysiology is compared before and after expertise is acquired, are increasingly being used as models for understanding the human brain's potential for reorganization. It is proving difficult to use these results to answer basic and important questions like how task training leads to both specific and general changes in behavior and how these changes correspond with modifications in the brain. The main culprit is the diversity of paradigms used as complex task models. An assortment of activities ranging from juggling to deciphering Morse code has been reported. Even when working in the same general domain, few researchers use similar training models. New ways to meaningfully compare complex tasks are needed. We propose a method for characterizing and deconstructing the task requirements of complex training paradigms, which is suitable for application to both structural and functional neuroimaging studies. We believe this approach will aid brain plasticity research by making it easier to compare training paradigms, identify "missing puzzle pieces," and encourage researchers to design training protocols to bridge these gaps.

Effects of musical training and event probabilities on encoding of complex tone patterns.

BACKGROUND: The human auditory cortex automatically encodes acoustic input from the environment and differentiates regular sound patterns from deviant ones in order to identify important, irregular events. The Mismatch Negativity (MMN) response is a neuronal marker for the detection of sounds that are unexpected, based on the encoded regularities. It is also elicited by violations of more complex regularities and musical expertise has been shown to have an effect on the processing of complex regularities. Using magnetoencephalography (MEG), we investigated the MMN response to salient or less salient deviants by varying the standard probability (70%, 50% and 35%) of a pattern oddball paradigm. To study the effects of musical expertise in the encoding of the patterns, we compared the responses of a group of non-musicians to those of musicians. RESULTS: We observed significant MMN in all conditions, including the least salient condition (35% standards), in response to violations of the predominant tone pattern for both groups. The amplitude of MMN from the right hemisphere was influenced by the standard probability. This effect was modulated by long-term musical training: standard probability changes influenced MMN amplitude in the group of non-musicians only. CONCLUSION: This study indicates that pattern violations are detected automatically, even if they are of very low salience, both in non-musicians and musicians, with salience having a stronger impact on processing in the right hemisphere of non-musicians. Long-term musical training influences this encoding, in that non-musicians benefit to a greater extent from a good signal-to-noise ratio (i.e. high probability of the standard pattern), while musicians are less dependent on the salience of an acoustic environment.

Musical expertise induces audiovisual integration of abstract congruency rules.

Perception of everyday life events relies mostly on multisensory integration. Hence, studying the neural correlates of the integration of multiple senses constitutes an important tool in understanding perception within an ecologically valid framework. The present study used magnetoencephalography in human subjects to identify the neural correlates of an audiovisual incongruency response, which is not generated due to incongruency of the unisensory physical characteristics of the stimulation but from the violation of an abstract congruency rule. The chosen rule-"the higher the pitch of the tone, the higher the position of the circle"-was comparable to musical reading. In parallel, plasticity effects due to long-term musical training on this response were investigated by comparing musicians to non-musicians. The applied paradigm was based on an appropriate modification of the multifeatured oddball paradigm incorporating, within one run, deviants based on a multisensory audiovisual incongruent condition and two unisensory mismatch conditions: an auditory and a visual one. Results indicated the presence of an audiovisual incongruency response, generated mainly in frontal regions, an auditory mismatch negativity, and a visual mismatch response. Moreover, results revealed that long-term musical training generates plastic changes in frontal, temporal, and occipital areas that affect this multisensory incongruency response as well as the unisensory auditory and visual mismatch responses.

Musical training as a framework for brain plasticity: behavior, function, and structure.

Musical training has emerged as a useful framework for the investigation of training-related plasticity in the human brain. Learning to play an instrument is a highly complex task that involves the interaction of several modalities and higher-order cognitive functions and that results in behavioral, structural, and functional changes on time scales ranging from days to years. While early work focused on comparison of musical experts and novices, more recently an increasing number of controlled training studies provide clear experimental evidence for training effects. Here, we review research investigating brain plasticity induced by musical training, highlight common patterns and possible underlying mechanisms of such plasticity, and integrate these studies with findings and models for mechanisms of plasticity in other domains.

Evidence for training-induced plasticity in multisensory brain structures: an MEG study.

Multisensory learning and resulting neural brain plasticity have recently become a topic of renewed interest in human cognitive neuroscience. Music notation reading is an ideal stimulus to study multisensory learning, as it allows studying the integration of visual, auditory and sensorimotor information processing. The present study aimed at answering whether multisensory learning alters uni-sensory structures, interconnections of uni-sensory structures or specific multisensory areas. In a short-term piano training procedure musically naive subjects were trained to play tone sequences from visually presented patterns in a music notation-like system [Auditory-Visual-Somatosensory group (AVS)], while another group received audio-visual training only that involved viewing the patterns and attentively listening to the recordings of the AVS training sessions [Auditory-Visual group (AV)]. Training-related changes in cortical networks were assessed by pre- and post-training magnetoencephalographic (MEG) recordings of an auditory, a visual and an integrated audio-visual mismatch negativity (MMN). The two groups (AVS and AV) were differently affected by the training. The results suggest that multisensory training alters the function of multisensory structures, and not the uni-sensory ones along with their interconnections, and thus provide an answer to an important question presented by cognitive models of multisensory training.