A neuroimaging study of phonological and semantic processing in healthy ageing and patients with primary progressive aphasia
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2025
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A strong interest in cognitive neuroscience lies in understanding how and where language processing occurs in the brain (Fridriksson et al., 2016). The widely accepted model for studying language processing, proposed by Hickok and Poeppel (Hickok & Poeppel, 2004, 2007), describes a dual-route network: the dorsal and the ventral streams. The dorsal stream connects temporal and frontal regions and is primarily lateralized to the left hemisphere. The ventral stream is a bilateral pathway (recruiting both the left and right hemispheres) and connects frontal regions to the parietal, temporal, and occipital lobes. These streams have been studied through verbal fluency (VF) tasks, with the dorsal stream associated with phonological processing and the ventral stream linked with semantic processing (Jobard et al., 2003).According to the dual-route network, many functional MRI (fMRI) studies on language processing report conflicting findings regarding the brain areas responsible for phonological and semantic processing (PP and SP, respectively). Some investigations (McDermott et al., 2003; Rimol et al., 2005; Sekiyama et al., 2003) using fMRI suggest that the inferior frontal gyrus, superior temporal gyrus, and middle temporal gyrus are activated during both types of processing. Indeed, Abrahams et al. (2003) and Heim et al. (2008) suggest that Broca's area is activated during both PP and SP tasks. However, other fMRI studies report significant differences in the brain areas associated with each type of processing. For example, Broca's area appears to be activated only during PP (S. Wagner et al., 2014), while the posterior left middle frontal gyrus is activated only during SP (Zhuang et al., 2016). In addition, findings by Meinzer et al. (2009) indicate that another brain region, such as the precuneus, shows significant activation during language processing, but exclusively during SP tasks. A subsequent study by Strijkers et al. (2017), employing magnetoencephalography and structural MRI, proposed the existence of a unified neural network underlying both types of processing, thereby supporting the notion of parallel processing. This finding highlights the absence of brain areas exclusively dedicated to PP and SP. Language abilities change and often decline with age, affecting both phonological and semantic levels of processing (Gordon & Kindred, 2011; Kavé & Knafo-Noam, 2015). Some authors (James & Burke, 2000; Taylor & Burke, 2002), however, suggest that PP and SP do not undergo age-related decline and may even improve with aging. PP and SP are of significant interest in the context of pathological aging, particularly for understanding language impairments associated with dementia (Olmos-Villaseñor et al., 2023). This is especially relevant in Primary Progressive Aphasia (PPA), an atypical neurodegenerative condition characterized by language processing deterioration (Tee & Gorno-Tempini, 2019). Specific linguistic deficits form part of the diagnostic criteria for PPA (Marshall et al., 2018). A more recent systematic review highlights that SP and PP could serve as early markers for this neurodegenerative condition and other dementia subtypes (Toloza-Ramírez et al., 2021).Functional fMRI is the preferred technique in cognitive neuroscience for studying language processing in the brain. Understanding the neural basis of language processing is essential for evaluating the effects of aging and for improving diagnostic criteria for neurodegenerative conditions such as PPA (M. L. Henry et al., 2018; Rotte, 2005). Through the current language processing model proposed by Hickok and Poeppel (2004, 2007), it is possible to identify relevant brain areas underlying SP and PP. However, this model (the dual-route network) is limited in explaining how these brain areas interact and modulate one another during VF tasks across different stages of aging and under neurodegenerative conditions. Future research should consider not only the neural basis of language processing but also the interconnection of brain regions using innovative models such as Dynamic Causal Modeling (DCM). DCM enables researchers to examine how regions within a network interact, revealing the functional integration and modulation of specific cortical pathways (K. J. Friston et al., 2003), especially in healthy aging and clinical populations. This approach could provide a better diagnostic framework, not limited to classical cognitive domains such as memory or executive functions, or to structural damage alone.This PhD proposal aims to study changes in activation and connectivity patterns for PP and SP in healthy older volunteers and patients with PPA. Likewise, it is also proposed that the effective connectivity of DCM be studied for both types of linguistic processing in normal aging and clinical populations.
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Tesis (Doctorate degree in Neurosciences)--Pontificia Universidad Católica de Chile, 2025.