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      Temporal selectivity declines in the aging human auditory cortex

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          Abstract

          Current models successfully describe the auditory cortical response to natural sounds with a set of spectro-temporal features. However, these models have hardly been linked to the ill-understood neurobiological changes that occur in the aging auditory cortex. Modelling the hemodynamic response to a rich natural sound mixture in N = 64 listeners of varying age, we here show that in older listeners’ auditory cortex, the key feature of temporal rate is represented with a markedly broader tuning. This loss of temporal selectivity is most prominent in primary auditory cortex and planum temporale, with no such changes in adjacent auditory or other brain areas. Amongst older listeners, we observe a direct relationship between chronological age and temporal-rate tuning, unconfounded by auditory acuity or model goodness of fit. In line with senescent neural dedifferentiation more generally, our results highlight decreased selectivity to temporal information as a hallmark of the aging auditory cortex.

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          It can often be difficult for an older person to understand what someone is saying, particularly in noisy environments. Exactly how and why this age-related change occurs is not clear, but it is thought that older individuals may become less able to tune in to certain features of sound.

          Newer tools are making it easier to study age-related changes in hearing in the brain. For example, functional magnetic resonance imaging (fMRI) can allow scientists to ‘see’ and measure how certain parts of the brain react to different features of sound. Using fMRI data, researchers can compare how younger and older people process speech. They can also track how speech processing in the brain changes with age.

          Now, Erb et al. show that older individuals have a harder time tuning into the rhythm of speech. In the experiments, 64 people between the ages of 18 to 78 were asked to listen to speech in a noisy setting while they underwent fMRI. The researchers then tested a computer model using the data. In the older individuals, the brain’s tuning to the timing or rhythm of speech was broader, while the younger participants were more able to finely tune into this feature of sound. The older a person was the less able their brain was to distinguish rhythms in speech, likely making it harder to understand what had been said.

          This hearing change likely occurs because brain cells become less specialised overtime, which can contribute to many kinds of age-related cognitive decline. This new information about why understanding speech becomes more difficult with age may help scientists develop better hearing aids that are individualised to a person’s specific needs.

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          Most cited references61

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          Ridge Regression: Biased Estimation for Nonorthogonal Problems

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            Identifying natural images from human brain activity.

            A challenging goal in neuroscience is to be able to read out, or decode, mental content from brain activity. Recent functional magnetic resonance imaging (fMRI) studies have decoded orientation, position and object category from activity in visual cortex. However, these studies typically used relatively simple stimuli (for example, gratings) or images drawn from fixed categories (for example, faces, houses), and decoding was based on previous measurements of brain activity evoked by those same stimuli or categories. To overcome these limitations, here we develop a decoding method based on quantitative receptive-field models that characterize the relationship between visual stimuli and fMRI activity in early visual areas. These models describe the tuning of individual voxels for space, orientation and spatial frequency, and are estimated directly from responses evoked by natural images. We show that these receptive-field models make it possible to identify, from a large set of completely novel natural images, which specific image was seen by an observer. Identification is not a mere consequence of the retinotopic organization of visual areas; simpler receptive-field models that describe only spatial tuning yield much poorer identification performance. Our results suggest that it may soon be possible to reconstruct a picture of a person's visual experience from measurements of brain activity alone.
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              Age-Related Changes in 1/f Neural Electrophysiological Noise.

              Aging is associated with performance decrements across multiple cognitive domains. The neural noise hypothesis, a dominant view of the basis of this decline, posits that aging is accompanied by an increase in spontaneous, noisy baseline neural activity. Here we analyze data from two different groups of human subjects: intracranial electrocorticography from 15 participants over a 38 year age range (15-53 years) and scalp EEG data from healthy younger (20-30 years) and older (60-70 years) adults to test the neural noise hypothesis from a 1/f noise perspective. Many natural phenomena, including electrophysiology, are characterized by 1/f noise. The defining characteristic of 1/f is that the power of the signal frequency content decreases rapidly as a function of the frequency (f) itself. The slope of this decay, the noise exponent (χ), is often <-1 for electrophysiological data and has been shown to approach white noise (defined as χ = 0) with increasing task difficulty. We observed, in both electrophysiological datasets, that aging is associated with a flatter (more noisy) 1/f power spectral density, even at rest, and that visual cortical 1/f noise statistically mediates age-related impairments in visual working memory. These results provide electrophysiological support for the neural noise hypothesis of aging. Significance statement: Understanding the neurobiological origins of age-related cognitive decline is of critical scientific, medical, and public health importance, especially considering the rapid aging of the world's population. We find, in two separate human studies, that 1/f electrophysiological noise increases with aging. In addition, we observe that this age-related 1/f noise statistically mediates age-related working memory decline. These results significantly add to this understanding and contextualize a long-standing problem in cognition by encapsulating age-related cognitive decline within a neurocomputational model of 1/f noise-induced deficits in neural communication.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                03 July 2020
                2020
                : 9
                : e55300
                Affiliations
                [1]Department of Psychology, University of Lübeck LübeckGermany
                University of Western Ontario Canada
                Carnegie Mellon University United States
                University of Western Ontario Canada
                University of Maryland United States
                Author information
                https://orcid.org/0000-0002-3440-7269
                http://orcid.org/0000-0002-9356-2234
                http://orcid.org/0000-0002-7619-0459
                Article
                55300
                10.7554/eLife.55300
                7410487
                32618270
                8696e863-fdd0-4f43-b06d-031a3aa95696
                © 2020, Erb et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 20 January 2020
                : 02 July 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: ERC-CoG-2014-646696 "AUDADAPT"
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: OB 352/2-1
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                The aged human auditory cortex shows preserved tonotopy, but temporal modulations are represented with a markedly broader tuning, highlighting decreased temporal selectivity as a hallmark of the aging auditory cortex.

                Life sciences
                functional mri,healthy aging,spectro-temporal modulations,hearing loss,presbycusis,temporal rate coding,human

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