Motor learning and memory consolidation: Cardiovascular fitness level impact and underlying prefrontal cortex hemodynamics

Abstract

[eng] Physical activity and cardiovascular exercise significantly impact brain structure and function. This effect is attributed to physiological factors like growth factor regulation (Cotman et al., 2007; El-Sayes et al., 2019; Feter et al., 2019; Roberta et al., 2020; Taubert et al., 2015; Voss et al., 2013), blood flow and cerebral oxygenation (Moriarty et al., 2019), promoting neuroplasticity and motor learning (Dayan & Cohen, 2011; Doyon & Benali, 2005). The cardiovascular fitness level modulates this impact (Pesce, 2012), with higher aerobic capacity linked to greater cerebral oxygenation (Salzman et al., 2022), and enhanced cognitive functions such as executive control (Dupuy et al., 2015; Hillman et al., 2008) or memory (Erickson et al., 2009; Loprinzi et al., 2023). These processes rely on the prefrontal cortex (PFC), a region highly responsive to exercise (Colcombe & Kramer, 2003; Hillman et al., 2008; Salzman et al., 2022). This thesis investigates the relationship between motor performance and cortical activity during motor learning and memory consolidation, considering the role of cardiovascular fitness level and sex differences. A rotational visuomotor adaptation task (rVMA) was used, while functional near-infrared spectroscopy (fNIRS) recorded right PFC activity during adaptation and retention phases. Results showed successful learning and consolidation, with improvements observed 1h post-learning. Based on hemodynamic data, we inferred coordinated explicit and implicit processes during adaptation, while retention strategies varied over time. 1h post-learning, implicit processes dominated; at 24h post-learning, both explicit and implicit processes were engaged. Regarding sex differences, men and women initially relied on implicit learning. However, PFC activation increased in men (explicit processes) before returning to implicit learning, while women sustained PFC activation (explicit processes). A similar pattern emerged during retention: 1h post-adaptation, both cohorts used implicit processes, but over time, women showed increased PFC activation (explicit processes); at 24h post-adaptation, men shifted to implicit learning, while women maintained explicit strategies. Cardiovascular fitness did not influence motor performance but affected learning dynamics. High-fit individuals transitioned from implicit to explicit learning, before reverting to implicit learning in later stages. In contrast, low-fit participants initially relied more on implicit processes, but later increased PFC activation (explicit processes). During retentions, high-fit individuals showed lower PFC activation (implicit processes), while low-fit individuals alternated between explicit and implicit processes. These findings provide new insights into continuous behavioral and cortical response analysis during motor learning and memory consolidation. Suggesting that cardiovascular fitness does not directly impact motor performance but modulates learning strategies. Moreover, men and women adopt different learning strategies, highlighting the importance of considering fitness levels and sex differences in future research on motor control field.

[spa] En esta tesis se estudia la relación entre la ejecución motora y la actividad cortico-cerebral subyacente durante el aprendizaje y evaluación de la consolidación de una tarea motora, considerando el impacto de la condición física y el sexo. Se utilizó una tarea de adaptación visomotora rotacional (rVMA) y espectroscopia funcional del infrarrojo cercano (fNIRS) para medir la actividad del córtex prefrontal (PFC). Los resultados indican que operan procesos de aprendizaje explícitos e implícitos, inferidos por la activación del PFC. La condición física y el sexo no afectan a la ejecución motora, pero sí a las estrategias de aprendizaje utilizadas. Estos hallazgos destacan la importancia de la condición física y el sexo en la función cognitiva, aportando nuevas perspectivas para la investigación en el campo del control motor.