Parkinson’s disease (PD) is defined by motor dysfunctions due to progressive neurodegeneration of nigrostriatal dopaminergic neurons caused by intracellular Lewy bodies containing alpha-synuclein (Braak et al., 2003) and, often, Alzheimer’s disease (AD) pathologies such as brain amyloid-beta and hyperphosphorylated tau toxic proteins (Parkkinen et al., 2008, Irwin et al., 2013). Pathological spread from the brainstem to limbic-neocortical regions induces PD-related dementia (PDD), characterized by severe cognitive deficits and disabilities in daily living activities (Halliday et al., 2008). In the same line, dementia with Lewy bodies (DLB) is characterized by intracellular Lewy bodies (mainly α-synuclein and ubiquitin aggregates) in the brain and, in many cases, co-AD neuropathology (Rongve et al., 2010). DLB patients have a particularly severe prognosis, including worse quality of life, higher health-related costs, shorter time to institutionalization, more severe caregiver burden, and shorter survival, with a deleterious social and financial impact (Rongve et al., 2010).

As a result of neuropathological/neurodegenerative processes, the dysfunction of frontostriatal, mesocortical, mesolimbic, and frontoparietal neural circuits, as revealed by dopamine neuroimaging and magnetic resonance imaging (MRI), may lead to cognitive deficits especially involving vigilance and frontal executive functions in PDD (Lin et al., 2021, Zarifkar et al., 2021) and DLB (Morbelli et al., 2019, Oppedal et al., 2019) patients. In contrast, ADD patients are typically characterized by prominent memory impairment, primarily episodic memory related to the hippocampus and medial temporal lobe functions (Dubois et al., 2014, Wolk and Dickerson, 2016).

Cognitive performance is based on the temporal synchronization of the neural activity within several task-specific brain regions, so electroencephalographic (EEG) techniques have an ideal millisecond-based time resolution to probe those cognitive systems at work. In this line, analyzing event-related EEG oscillations (EROs) in PDD and DLB patients during an oddball task is especially promising (Güntekin & Başar, 2016). Indeed, this task requires that instructed participants quickly and accurately react to infrequent (visual or auditory) target stimuli (20-30%) intermingled with frequent (80-70%) stimuli, a performance based on frontal executive functions (Güntekin & Başar, 2016). Furthermore, the oddball ERO delta (< 4 Hz) and theta (4-7 Hz) responses underpin frontal executive functions typically affected in PDD and DLB patients (i.e., focused attention, perception, short-term memory, rule-based decision-making, and sensorimotor transformations), and increase in amplitude as a function of the task-related cognitive load (Başar-Eroglu et al., 1992, Harmony et al., 1996). In this line, Güntekin et al. (2018) investigated auditory oddball delta responses in PD patients without cognitive impairment, PD patients with mild cognitive impairment (PDMCI), and PDD patients at the group level. Results showed that ERO delta responses were lower in PD patients than in healthy control (HC) participants as a function of their cognitive impairment. Furthermore, Yener et al. (2019) reported lower visual oddball ERO theta phase-locking in ADMCI and PDMCI patients than in HC participants, with the most significant effects in PDMCI patients. Other ERO studies showed similar results in PDD patients (Pugnetti et al., 2010, Güntekin et al., 2018, Güntekin et al., 2020).

However, not all studies confirmed the presence of more significant differences in the oddball EROs in PDD-DLB patients compared to ADD patients. Specifically, several previous studies using auditory and visual oddball paradigms repeatedly reported lower oddball ERO responses at delta (< 4 Hz) and theta (4-7 Hz) frequency bands not only in PDD and DLB patients but also in ADD patients (Yener et al., 2007, Yener et al., 2008, Yener et al., 2012, Yener et al., 2013, Yener et al., 2014, Yener et al., 2016, Yener et al., 2019, Başar et al., 2010, Caravaglios et al., 2008, Caravaglios et al., 2010, Dushanova, 2011, Liu et al., 2012, Kurt et al., 2014, Emek-Savaş et al., 2017, Güntekin et al., 2008, Güntekin et al., 2018, Güntekin et al., 2020, Güntekin et al., 2022, Rosenblum et al., 2020, Rosenblum et al., 2022a, Rosenblum et al., 2022b, Tülay et al., 2020, Bayraktaroğlu et al., 2022, Hünerli-Gündüz et al., 2022). Furthermore, Tülay et al. (2020) reported lower visual oddball ERO delta responses in ADMCI and ADD patients than in HC participants. Other studies showed lower auditory and visual oddball ERO theta responses in all PD, ADD, and DLB patients than in HC participants (Schmiedt et al., 2005, Missonnier et al., 2006, Yener et al., 2007, Caravaglios et al., 2010, Singh et al., 2018, Tülay et al., 2020, Rosenblum et al., 2020, Rosenblum et al., 2022a, Rosenblum et al., 2022b, Güntekin et al., 2020, Güntekin et al., 2022; Rosenblum et al., 2020; 2022a; 2022b).

A limit of the above studies is that oddball ERO delta and theta responses were only sometimes compared in groups of ADD, PDD, and DLB patients with matched demographical variables and cognitive status. Furthermore, the topography of the ERO effects was only sometimes considered. Finally, most studies used only visual or auditory oddball stimuli, making a supramodal analysis of the impact impossible. To tackle these issues, the present study aimed to test the hypothesis that there may be greater changes in oddball ERO delta and theta responses in frontal areas in PDD and DLB patients than in ADD patients. This effect may be supramodal as high-order frontal executive functions are expected to be dysregulated in PDD and DLB patients.