Language comprehension in healthy ageing and mild cognitive impairment

Despite structural decline in language relevant brain regions, language comprehension appears to be relatively preserved with age. This raises the question: “How does the ageing brain maintain the cognitive system?” In this context, this thesis investigates the behavioural and functional underpinnings of sentence comprehension in healthy ageing and Mild Cognitive Impairment (MCI). Using a minimal phrase paradigm designed to focus on the process of syntactic binding, Chapter 1 reports a behavioural experiment demonstrating age-related decline in syntactic comprehension that increases in the absence of semantic-contextual information. Extending on these findings, Chapter 2 reports an electroencephalography (EEG) experiment on the oscillatory mechanisms involved in syntactic processing in older adults, which gives evidence for qualitative differences in the neural signature associated with syntactic binding in older compared to younger adults. Chapter 3 reports an EEG experiment on oscillatory activity associated with lexical retrieval and semantic processing in MCI. The results indicate subtle, yet clear alterations in the neural signatures associated with these processes in individuals with MCI relative to healthy controls. Collectively, the studies reported in this thesis add to our understanding of the robustness and changeability of the language comprehension system in the face of the wide array of changes that occur with ageing, further constraining neurocognitive theories on this subject

Neural dynamics of selective attention to speech in noise

This thesis investigates how the neural system instantiates selective attention to speech in challenging acoustic conditions, such as spectral degradation and the presence of background noise. Four studies using behavioural measures, magneto- and electroencephalography (M/EEG) recordings were conducted in younger (20–30 years) and older participants (60–80 years). The overall results can be summarized as follows. An EEG experiment demonstrated that slow negative potentials reflect participants’ enhanced allocation of attention when they are faced with more degraded acoustics. This basic mechanism of attention allocation was preserved at an older age. A follow-up experiment in younger listeners indicated that attention allocation can be further enhanced in a context of increased task-relevance through monetary incentives. A subsequent study focused on brain oscillatory dynamics in a demanding speech comprehension task. The power of neural alpha oscillations (~10 Hz) reflected a decrease in demands on attention with increasing acoustic detail and critically also with increasing predictiveness of the upcoming speech content. Older listeners’ behavioural responses and alpha power dynamics were stronger affected by acoustic detail compared with younger listeners, indicating that selective attention at an older age is particularly dependent on the sensory input signal. An additional analysis of listeners’ neural phase-locking to the temporal envelopes of attended speech and unattended background speech revealed that younger and older listeners show a similar segregation of attended and unattended speech on a neural level. A dichotic listening experiment in the MEG aimed at investigating how neural alpha oscillations support selective attention to speech. Lateralized alpha power modulations in parietal and auditory cortex regions predicted listeners’ focus of attention (i.e., left vs right). This suggests that alpha oscillations implement an attentional filter mechanism to enhance the signal and to suppress noise. A final behavioural study asked whether acoustic and semantic aspects of task-irrelevant speech determine how much it interferes with attention to task-relevant speech. Results demonstrated that younger and older adults were more distracted when acoustic detail of irrelevant speech was enhanced, whereas predictiveness of irrelevant speech had no effect. All findings of this thesis are integrated in an initial framework for the role of attention for speech comprehension under demanding acoustic conditions

Neural signatures of task-related fluctuations in auditory attention change with age

Listening in everyday life requires attention to be deployed dynamically – when listening is expected to be difficult and when relevant information is expected to occur – to conserve mental resources. Conserving mental resources may be particularly important for older adults who often experience difficulties understanding speech. We use electro- and magnetoencephalography to investigate the neural and behavioral mechanics of dynamic attention regulation during listening and the effects that aging may have on these. We show that neural alpha oscillatory activity indicates when in time attention is deployed (Experiment 1) and that deployment depends on listening difficulty (Experiment 2). Older adults also show successful attention regulation, although younger adults appear to utilize timing information a bit differently compared to older adults. We further show that the recruited brain regions differ between age groups. Superior parietal cortex is involved in attention regulation in younger adults, whereas posterior temporal cortex is more involved in older adults (Experiment 3). This difference in the sources of alpha activity across age groups was only observed when a task was performed, and not for alpha activity during resting-state recordings (Experiment S1). In sum, our study suggests that older adults employ different neural control strategies compared to younger adults to regulate attention in time under listening challenges

Cambios relacionados coa idade na actividade eléctrica cerebral diante dunha tarefa de memoria de traballo viso-espacial

O declive das capacidades cognitivas asociado á idade afecta principalmente á memoria de traballo viso-espacial, polo que afondar no coñecemento sobre os seus aspectos básicos e a súa evolución ó longo da vida é esencial para xerar intervencións que propicien melloras na calidade de vida dos maiores. Consecuentemente, nesta tese de doutoramento analizouse o sinal electroencefalográfico durante a codificación, mantemento e recuperación da información en memoria de traballo viso-espacial. Deste xeito, estudouse tanto a estrutura temporal da actividade eléctrica cerebral, e a súa modulación por manipulacións da carga en memoria e da duración do mantemento; como o impacto do avellentamento en dita actividade. Os resultados amosaron que a estrutura temporal da actividade eléctrica cerebral durante a codificación e recuperación é semellante, abranguendo dende procesos perceptivos ata procesos post-categorización do estímulo. Manipulacións da carga en memoria modularon a asignación de recursos de procesamento para procesos de avaliación e categorización dos estímulos, así como para procesos postcategorización. En tanto que as manipulacións da duración do mantemento, modularon os recursos de procesamento recrutados por procesos perceptivos e de avaliación estimular durante a recuperación. Pola súa parte, o mantemento de información caracterizouse por un aumento da inhibición en áreas cerebrais irrelevantes para a tarefa, concorrente cunha redución dependente da carga na inhibición en áreas relevantes. En canto ó avellentamento, existe unha diminución da velocidade en diferentes aspectos da avaliación estimular durante a codificación e a recuperación. Tamén se observou maior dependencia do recrutamento dos recursos de procesamento frontais en relación ós parietais nos maiores. Amais, durante o mantemento de información apreciouse unha ineficiente coordinación, asociada á idade, das redes neurais relevante e irrelevante para a tarefa, que se caracterizou por un déficit na inhibición da rede irrelevante para a tarefa, asociado co deterioro da execución condutual

Brain Rhythms and Working Memory in Healthy Ageing

Working memory (WM), the ability to maintain and manipulate information to guide immediate cognitive processing, is vulnerable to age-related decline. Compared with younger adults, older adults demonstrate smaller WM capacities, a decrease in the ability to manipulate items held in WM, and a greater susceptibility to interference from distracting information. However, the neural underpinnings of WM decline in normal ageing are unclear. One technique that can be used to investigate the neurophysiological processes underlying cognition is electroencephalography (EEG), which non-invasively records activity from the awake human brain. The research described in this thesis uses EEG to investigate the neurophysiology of WM in healthy younger and older adults, with a particular focus on neural oscillatory activity in the alpha frequency range (8-12 Hz). As such, Chapter 1 consists of a review of the literature relevant to use of EEG to investigate the neurophysiology of WM performance in younger and older adults. WM performance deficits in older adults are particularly salient under increasing WM loads. Alpha oscillations have been shown to support verbal WM performance under high loads in younger adults, so the aim of Chapter 2 was to investigate the load-dependent modulation of alpha oscillatory power and frequency in younger and older adults during verbal WM. No age differences in verbal WM performance were found, and alpha power and alpha peak frequency were modulated in a similar task- and load-dependent manner in both younger and older adults. Another factor influencing WM performance in older adults is a decline in selective attention. Older adults perform worse on and are less able to modulate alpha power than younger adults in tasks involving cues about ‘where’ or ‘when’ a memory set will appear. The study described in Chapter 3 investigated whether providing cues towards memory set presentation time led to enhanced selective attention before the onset of the memory set, as indexed by alpha oscillatory activity. Predictive cues led to improved WM performance in both age groups, but alpha power in preparation of the memory set did not influence task performance. In Chapter 3, there were no age differences in WM performance when manipulating memory set presentation time. However, processing speed may not only limit the speed at which items are encoded into WM, but also the speed at which stimuli are transformed into a stable memory representation (i.e., WM consolidation). Therefore, the study contained in Chapter 4 investigated age differences in the ability to consolidate items into visual WM. In this study, older adults demonstrated poorer WM performance and slower consolidation at low WM loads, providing evidence for altered visual WM consolidation with age. Finally, visual WM is severely limited in capacity, highlighting the importance of encoding task-relevant information while ignoring distractors. The modulation of alpha oscillatory power has been implicated in the inhibition of distractors during WM in younger adults, but it is unclear if alpha power modulation also supports distractor inhibition in older adults. The study described in Chapter 5 investigated age differences in alpha oscillatory power before the onset of distractors during the visual WM retention period. Although there were no age differences in WM performance, younger adults demonstrated functionally relevant increases in alpha power before distractors, while older adults showed decreases in alpha power. Therefore, younger and older adults likely use different neural strategies to inhibit distractors during WM performance. Taken together, the results of the studies contained in this thesis provide further evidence for age-related changes to neural oscillatory activity, particularly in the alpha frequency band, even when age differences in WM performance are not present. These findings may have important implications for providing novel targets for detecting or preventing age-related cognitive decline.Thesis (Ph.D.) -- University of Adelaide, School of Biomedicine, 202

Investigating the neural mechanisms underlying auditory and audio-visual perception in younger and older adults

This thesis aimed to address questions in two distinct areas of research in ageing and cognitive neuroscience. Firstly, given that the pre-stimulus state of cortical oscillations had been shown to predict behavioural and neural responses, we addressed the question of whether pre-stimulus oscillatory mechanisms change or remain consistent in the ageing brain. Secondly, previous research had shown that Audio-visual (AV) speech influences the amplitude and latency of evoked activity. Our research addressed the questions of whether/how AV enhancement and visual predictability of AV speech is represented in evoked activity in noisy listening conditions, and whether such Electroencephalographic (EEG) signatures remain stable with age. In Chapter 3 we investigated the consistency of how pre-stimulus activity influences auditory frequency discrimination performance in young and older participants. In both groups the power of pre-stimulus activity influenced the encoding of sensory evidence reflected by early evoked components, while the phase influenced choice formation in later-activated EEG components. Importantly, for the early EEG components we did not find evidence for a systematic difference in the time scales of the perceptually relevant pre-stimulus activity. In the later-activated EEG component we found a trend for perceptually relevant rhythmic activity to arise from slower frequencies in the ageing brain. At the same time our data replicate previous findings of a significant age-related slowing of Auditory Evoked Potential (AEP) latency, modulations of AEP amplitudes, and a flattening of the spectral profile of EEG activity. In Chapter 4, we investigated the consistency of behaviour and evoked activity underlying AV speech integration in a speech-in-noise discrimination task in younger and older adults. Behaviourally, younger and older adults performed comparably. Performance was greater for Audio-visually informative (AVinf) speech compared to Auditory-only informative (AOinf) speech across groups and noise levels, and was poorer at low noise levels. AV enhancement was greater in high noise levels, across all participants, and older adults derived greater AV enhancement compared to younger adults (an effect that was consistent across noise levels). In terms of visual predictability, we found that word discrimination performance was greater for target words with non-labial initial phonemes (assumed least visually predictive), compared to labial initial phonemes (assumed most visually predictive). Furthermore, we found that AV enhancement was greater for labial initial phonemes, compared to non-labial initial phonemes, and this was consistent across age groups.Neurally, we found that AV enhancement is represented by a centro-parietal P3-like activity in older adults and an N4-like fronto-central activity in younger adults, but found that this activity did not correlate with behavioural AV enhancement. Our results point to distinct patterns of late evoked activity underlying AV enhancement between younger and older adults, possibly representing distinct cognitive (memory) strategies in predicting upcoming target stimuli. At the same time our data replicate previous findings of a significant age-related slowing of AEP latency, modulations of AEP amplitudes, and a flattening of the spectral profile of EEG activity. In Chapter 5 we investigated the consistency of evoked activity underlying the visual predictability of AV speech. We found that visual predictability was reflected by late fronto-central negativity in older adults, but not in younger adults. However, we did not find evidence of an interaction between visual predictability and AV enhancement in terms of evoked activity, raising further questions about how visual predictability of speech is represented the brain’s electrophysiology. Our results point to distinct patterns of late evoked activity underlying visual predictability of visual speech, again possibly reflecting differential strategies in predictive coding. In summary, the results of this thesis demonstrate that pre-stimulus mechanisms in auditory pitch perception remain consistent in the younger and older adult brain, while spectral dynamics change with age. Our results also replicate previous work demonstrating age-related delays in peak latency, and changes in peak amplitude, of early auditory evoked activity. And lastly, we demonstrate that differences in the EEG signatures of AV enhancement between younger and older adults emerge in late evoked activity, and that visual predictability of speech is represented in late evoked activity only in older adults

Characterizing the Influence of Perturbations in Global State on Working Memory

When accomplishing goal-directed behavior in naturalistic settings our globalphysiological state can vary dramatically, oscillating between periods of wakefulness, emotional stress, and physical activity. Fluctuations in global state, in turn, induce a cascade of neuromodulatory changes that affect how the brain processes sensory information from the external environment. Despite the inextricable link between global state and brain function, goal-directed behavior has predominantly been studied when the body is stationary and at rest. Thus, it is unclear as to whether perturbations in global state modulate cognitive processes dependent on this sensory information, such as working memory (WM). The current body of work aims to determine how changes in global state induced by an acute bout of aerobic exercise modulate WM and its underlying neural correlates. Study 1 investigated the relationship between acute exercise and cognition, which revealed that aerobic exercise induces a small enhancement in general task-performance. Moderator analyses indicated that time-dependent measures of cognition were especially improved by exercise-induced perturbations in global state. Importantly, executive functions, such as inhibitory control and WM, were influenced by engaging in physical activity. Building on these meta-analytic results, Study 2 investigated whether the fidelity of spatial WM representations is impacted during an instance of aerobic exercise. Participants completed a delayed change detection task both at rest and during a bout of low-intensity cycling while neural activity was concurrently recorded using electroencephalography (EEG). An inverted encoding modeling technique was employed to estimate location-selective channel response functions from topographical patterns of alpha-band (8-12 Hz) activity. Importantly, robust spatially selective responses were reconstructed both at rest and during exercise throughout the stimulus encoding and retention period, demonstrating for the first time that the fidelity of spatial WM representations could be tracked in a physiologically active state. The selectivity of these responses was degraded during exercise relative to rest, suggesting that the fidelity of location representations may be diminished. Study 3 further investigated the impact of exercise on WM encoding and maintenance abilities. Participants completed a delayed change detection task that consisted of varying set sizes. Importantly, on some of the trials participants were required to encode target stimuli while simultaneously ignoring distractors, thus enabling the evaluation of WM filtering efficiency. Analyses of an event-related potential known as contralateral delay activity (CDA), which tracks the number of items stored in WM, indicated that there was no difference in WM load between rest and exercise conditions. Decoding analyses revealed that patterns of voltage potentials across the scalp tracked WM load both at rest and during exercise. These results suggest that WM filtering efficiency and the number of items that can be actively stored are robust to perturbations in global state caused by light intensity exercise. Together, this collection of studies illuminates the selective impact of exercise on WM processes, and highlights the importance of considering global state when developing theoretical frameworks of cognition