Longitudinal changes in auditory and reward systems following receptive music-based intervention in older adults.
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ABSTRACT:
SUBMITTER: Quinci MA
PROVIDER: S-EPMC9261172 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:As sensory stimuli and behavioral demands change, the attentive brain quickly identifies task-relevant stimuli and associates them with appropriate motor responses. The effects of attention on sensory processing vary across task paradigms, suggesting that the brain may use multiple strategies and mechanisms to highlight attended stimuli and link them to motor action. To better understand factors that contribute to these variable effects, we studied sensory representations in primary auditory cortex (A1) during two instrumental tasks that shared the same auditory discrimination but required different behavioral responses, either approach or avoidance. In the approach task, ferrets were rewarded for licking a spout when they heard a target tone amid a sequence of reference noise sounds. In the avoidance task, they were punished unless they inhibited licking to the target. To explore how these changes in task reward structure influenced attention-driven rapid plasticity in A1, we measured changes in sensory neural responses during behavior. Responses to the target changed selectively during both tasks but did so with opposite sign. Despite the differences in sign, both effects were consistent with a general neural coding strategy that maximizes discriminability between sound classes. The dependence of the direction of plasticity on task suggests that representations in A1 change not only to sharpen representations of task-relevant stimuli but also to amplify responses to stimuli that signal aversive outcomes and lead to behavioral inhibition. Thus, top-down control of sensory processing can be shaped by task reward structure in addition to the required sensory discrimination.
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Project description:Music can evoke pleasurable and rewarding experiences. Past studies that examined task-related brain activity revealed individual differences in musical reward sensitivity traits and linked them to interactions between the auditory and reward systems. However, state-dependent fluctuations in spontaneous neural activity in relation to music-driven rewarding experiences have not been studied. Here, we used functional MRI to examine whether the coupling of auditory-reward networks during a silent period immediately before music listening can predict the degree of musical rewarding experience of human participants (N = 49). We used machine learning models and showed that the functional connectivity between auditory and reward networks, but not others, could robustly predict subjective, physiological, and neurobiological aspects of the strong musical reward of chills. Specifically, the right auditory cortex-striatum/orbitofrontal connections predicted the reported duration of chills and the activation level of nucleus accumbens and insula, whereas the auditory-amygdala connection was associated with psychophysiological arousal. Furthermore, the predictive model derived from the first sample of individuals was generalized in an independent dataset using different music samples. The generalization was successful only for state-like, pre-listening functional connectivity but not for stable, intrinsic functional connectivity. The current study reveals the critical role of sensory-reward connectivity in pre-task brain state in modulating subsequent rewarding experience.
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Project description:ObjectiveTo investigate the effect of postoperative delirium on longitudinal brain microstructural changes, as measured by diffusion tensor imaging.MethodsWe studied a subset of the larger Successful Aging after Elective Surgery (SAGES) study cohort of older adults (≥70 years) without dementia undergoing elective surgery: 113 participants who had diffusion tensor imaging before and 1 year after surgery. Postoperative delirium severity and occurrence were assessed during the hospital stay using the Confusion Assessment Method and a validated chart review method. We investigated the association of delirium severity and occurrence with longitudinal diffusion changes across 1 year, adjusting for age, sex, vascular comorbidity, and baseline cognitive performance. We also assessed the association between changes in diffusion and cognitive performance across the 1-year follow-up period, adjusting for age, sex, education, and baseline cognitive performance.ResultsPostoperative delirium occurred in 25 participants (22%). Delirium severity and occurrence were associated with longitudinal diffusion changes in the periventricular, frontal, and temporal white matter. Diffusion changes were also associated with changes in cognitive performance across 1 year, although the cognitive changes did not show significant association with delirium severity or occurrence.ConclusionsOur study raises the possibility that delirium has an effect on the development of brain microstructural abnormalities, which may reflect brain changes underlying cognitive trajectories. Future studies are warranted to clarify whether delirium is the driving factor of the observed changes or rather a correlate of a vulnerable brain that is at high risk for neurodegenerative processes.
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Project description:Encoding properties of sensory neurons are commonly modeled using linear finite impulse response (FIR) filters. For the auditory system, the FIR filter is instantiated in the spectro-temporal receptive field (STRF), often in the framework of the generalized linear model. Despite widespread use of the FIR STRF, numerous formulations for linear filters are possible that require many fewer parameters, potentially permitting more efficient and accurate model estimates. To explore these alternative STRF architectures, we recorded single-unit neural activity from auditory cortex of awake ferrets during presentation of natural sound stimuli. We compared performance of > 1000 linear STRF architectures, evaluating their ability to predict neural responses to a novel natural stimulus. Many were able to outperform the FIR filter. Two basic constraints on the architecture lead to the improved performance: (1) factorization of the STRF matrix into a small number of spectral and temporal filters and (2) low-dimensional parameterization of the factorized filters. The best parameterized model was able to outperform the full FIR filter in both primary and secondary auditory cortex, despite requiring fewer than 30 parameters, about 10% of the number required by the FIR filter. After accounting for noise from finite data sampling, these STRFs were able to explain an average of 40% of A1 response variance. The simpler models permitted more straightforward interpretation of sensory tuning properties. They also showed greater benefit from incorporating nonlinear terms, such as short term plasticity, that provide theoretical advances over the linear model. Architectures that minimize parameter count while maintaining maximum predictive power provide insight into the essential degrees of freedom governing auditory cortical function. They also maximize statistical power available for characterizing additional nonlinear properties that limit current auditory models.
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Project description:Abstract Older adults with depression may manifest cognitive decline and treating depression may maintain or improve cognition. However, cognitive outcomes could be overlooked in non-pharmacological interventions for depression. This analysis investigated cognitive changes in a stepped-care intervention (Clinical Trial ID: NCT03593889) and the potential association with individual depressive symptom change. The community-dwelling older adults at risk of or with depressive symptoms without significant cognitive impairment (n=802) were assigned to intervention group (n=644) and control group (n=138). Depressive symptoms and cognitive functions were measured using Patient Health Questionnaire-9 and Cognitive Montreal Assessment-5 minutes protocol, respectively. Paired-t-Test showed significant improvements in overall cognition and attention in both intervention and control groups, but the improvements of language fluency (Intervention: MD=-0.51 p<0.01; control: MD=0.14, p=0.500) and orientation (Intervention: MD=-0.22 p<0.05; control: MD=-0.11, p=0.229) only displayed in intervention group. As control group had better cognition at baseline, linear mixed-effects model analysis was used to compare between-group difference. Intervention group had no significant cognitive improvement after adjusting the covariates but a potential improvement in language fluency (Coef. =0.442, SE=0.247, p=0.074). A linear regression analysis in intervention group indicated that reduction of concentration problem (β=0.106, p<0.05) and retardedness (β=0.117, p<0.01) under the symptomatology of depression were associated with the improvement of language fluency. In this group of older persons without significant cognitive impairment, there is no clear evidence of global cognitive benefits in a stepped care depression intervention, although there may be improvements in certain cognitive domains, which may be related to improvements in cognitive aspects of depression.
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Project description:Here we describe a method for measuring tonotopic maps and estimating bandwidth for voxels in human primary auditory cortex (PAC) using a modification of the population Receptive Field (pRF) model, developed for retinotopic mapping in visual cortex by Dumoulin and Wandell (2008). The pRF method reliably estimates tonotopic maps in the presence of acoustic scanner noise, and has two advantages over phase-encoding techniques. First, the stimulus design is flexible and need not be a frequency progression, thereby reducing biases due to habituation, expectation, and estimation artifacts, as well as reducing the effects of spatio-temporal BOLD nonlinearities. Second, the pRF method can provide estimates of bandwidth as a function of frequency. We find that bandwidth estimates are narrower for voxels within the PAC than in surrounding auditory responsive regions (non-PAC).
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Project description:Previous studies have shown that the auditory cortex can enhance the perception of behaviorally important sounds in the presence of background noise, but the mechanisms by which it does this are not yet elucidated. Rapid plasticity of spectrotemporal receptive fields (STRFs) in the primary (A1) cortical neurons is observed during behavioral tasks that require discrimination of particular sounds. This rapid task-related change is believed to be one of the processing strategies utilized by the auditory cortex to selectively attend to one stream of sound in the presence of mixed sounds. However, the mechanism by which the brain evokes this rapid plasticity in the auditory cortex remains unclear. This paper uses a neural network model to investigate how synaptic transmission within the cortical neuron network can change the receptive fields of individual neurons. A sound signal was used as input to a model of the cochlea and auditory periphery, which activated or inhibited integrate-and-fire neuron models to represent networks in the primary auditory cortex. Each neuron in the network was tuned to a different frequency. All neurons were interconnected with excitatory or inhibitory synapses of varying strengths. Action potentials in one of the model neurons were used to calculate the receptive field using reverse correlation. The results were directly compared to previously recorded electrophysiological data from ferrets performing behavioral tasks that require discrimination of particular sounds. The neural network model could reproduce complex STRFs observed experimentally through optimizing the synaptic weights in the model. The model predicts that altering synaptic drive between cortical neurons and/or bottom-up synaptic drive from the cochlear model to the cortical neurons can account for rapid task-related changes observed experimentally in A1 neurons. By identifying changes in the synaptic drive during behavioral tasks, the model provides insights into the neural mechanisms utilized by the auditory cortex to enhance the perception of behaviorally salient sounds.
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Project description:A central question in sensory neuroscience is how neurons represent complex natural stimuli. This process involves multiple steps of feature extraction to obtain a condensed, categorical representation useful for classification and behaviour. It has previously been shown that central auditory neurons in the starling have composite receptive fields composed of multiple features. Whether this property is an idiosyncratic characteristic of songbirds, a group of highly specialized vocal learners or a generic property of sensory processing is unknown. To address this question, we have recorded responses from auditory cortical neurons in mice, and characterized their receptive fields using mouse ultrasonic vocalizations (USVs) as a natural and ethologically relevant stimulus and pitch-shifted starling songs as a natural but ethologically irrelevant control stimulus. We have found that these neurons display composite receptive fields with multiple excitatory and inhibitory subunits. Moreover, this was the case with either the conspecific or the heterospecific vocalizations. We then trained the sparse filtering algorithm on both classes of natural stimuli to obtain statistically optimal features, and compared the natural and artificial features using UMAP, a dimensionality-reduction algorithm previously used to analyse mouse USVs and birdsongs. We have found that the receptive-field features obtained with both types of the natural stimuli clustered together, as did the sparse-filtering features. However, the natural and artificial receptive-field features clustered mostly separately. Based on these results, our general conclusion is that composite receptive fields are not a unique characteristic of specialized vocal learners but are likely a generic property of central auditory systems. KEY POINTS: Auditory cortical neurons in the mouse have composite receptive fields with several excitatory and inhibitory features. Receptive-field features capture temporal and spectral modulations of natural stimuli. Ethological relevance of the stimulus affects the estimation of receptive-field dimensionality.
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Project description:Music-based interventions (MBI) have become increasingly widely adopted for dementia and related disorders. Previous research shows that music engages reward-related regions through functional connectivity with the auditory system, but evidence for the effectiveness of MBI is mixed in older adults with mild cognitive impairment (MCI) and Alzheimer's disease (AD). This underscores the need for a unified mechanistic understanding to motivate MBIs. The main objective of the present study is to characterize the intrinsic connectivity of the auditory and reward systems in healthy aging individuals with MCI, and those with AD. Using resting-state fMRI data from the Alzheimer's Database Neuroimaging Initiative, we tested resting-state functional connectivity within and between auditory and reward systems in older adults with MCI, AD, and age-matched healthy controls (N = 105). Seed-based correlations were assessed from regions of interest (ROIs) in the auditory network (i.e., anterior superior temporal gyrus, posterior superior temporal gyrus, Heschl's Gyrus), and the reward network (i.e., nucleus accumbens, caudate, putamen, and orbitofrontal cortex). AD individuals were lower in both within-network and between-network functional connectivity in the auditory network and reward networks compared to MCI and controls. Furthermore, graph theory analyses showed that the MCI group had higher clustering and local efficiency than both AD and control groups, whereas AD individuals had lower betweenness centrality than MCI and control groups. Together, the auditory and reward systems show preserved within- and between-network connectivity in MCI individuals relative to AD. These results motivate future music-based interventions in individuals with MCI due to the preservation of functional connectivity within and between auditory and reward networks at that initial stage of neurodegeneration.
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