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Griffa, G.

Publications and source records attributed to Griffa, G..

3 recordsLinked to original sources

Distinct cellular processes drive motor skill learning in the human brain

Despite decades of research, the biological mechanisms by which motor skills consolidate in the human brain remain poorly understood. Diffusion MRI provides a unique opportunity to probe biological processes non-invasively, as water displacements occur on the micrometer scale. Using diffusion tensor imaging (DTI), our team showed that motor sequence learning (MSL) induces microstructural changes in the hippocampus and key motor regions, suggesting that declarative and procedural systems may operate as part of the same network. Yet DTI cannot identify the cellular source of these changes, leaving open whether they reflect structural plasticity --remodeling of dendritic and astrocytic processes described in rodents-- or transient homeostatic responses that accompany learning --neuronal and astrocytic swelling. Here, we combined ultra-high-gradient diffusion MRI with the compartment-based Soma and Neurite Density Imaging (SANDI) model to disentangle the cellular basis of motor skill memory consolidation. DTI showed that MSL induced rapid microstructural changes in the hippocampus, precuneus, and motor regions, but only those in the precuneus and posterior parietal cortex (PPC) persisted overnight. SANDI revealed that DTI changes were driven by two distinct cellular processes: a transient enlargement of the cell soma across all regions consistent with a short-lived homeostatic response, and a sustained rise in cell-process density restricted to the precuneus and PPC, compatible with structural plasticity. By decomposing diffusion signals into their cellular sources, our work disambiguates transient and enduring processes, providing the first non-invasive evidence for the cellular basis of human motor memory consolidation and a framework for studying neuroplasticity in vivo.

neuroscience↗

The human hippocampus is involved in implicit motor learning

Recent evidence suggests that the human hippocampus, traditionally associated with declarative memory, plays a role in motor sequence learning (MSL). However, the classic MSL paradigm depends initially on declarative learning. Therefore, it is critical to discern whether the participation of the hippocampus relates to its canonical role or to processing a general aspect of learning that transcends the declarative/non-declarative distinction. To address this issue, here we turn to visuomotor adaptation -a type of motor learning involving skill recalibration-which unlike MSL can be easily manipulated to eliminate the explicit component. Here, we examined the broader involvement of the hippocampus in procedural motor learning by using diffusion MRI to indirectly assess structural plasticity associated with memory consolidation in visuomotor adaptation (VMA) and an implicit-only version (IVMA). We found that both VMA and IVMA engaged the left posterior hippocampus in a learning-specific manner. Remarkably, while VMA induced only transient hippocampal alterations, IVMA elicited structural changes that persisted overnight, underscoring the reliance on implicit learning for enduring neuroplasticity. As expected, training on both visuomotor tasks impacted the microstructure of the cerebellum, the motor and the posterior parietal cortex. Notably, the temporal dynamics of changes in these regions closely paralleled those of the left hippocampus, suggesting that motor and limbic regions operate in a coordinated manner as part of the same neural network. Collectively, our findings support an active role of the hippocampus in procedural motor memory and argue for a unified function in memory encoding regardless of the declarative or non-declarative nature of the task.

neuroscience↗

Consolidation of sensorimotor adaptation depends both on the passage of time and sleep

Contrary to its well-established role in declarative learning the impact of sleep on motor memory consolidation remains a subject of debate. Motor learning involves skill acquisition and skill maintenance, two critical aspects in achieving movement precision. Current literature suggests that whereas motor skill acquisition benefits from sleep, consolidation of skill maintenance depends solely on the passage of time. This has led to the proposal that skill maintenance may be an exception to other types of memories. Here, we address this ongoing controversy in humans through three comprehensive experiments. We found that when training occurs throughout the day consolidation of skill maintenance proceeds independently of sleep. However, when it takes place closely before bedtime so that sleep aligns with the memory stabilization window, a 30% memory enhancement emerges along with a distinct modulation of neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in procedural motor learning, and offer the potential to accelerate motor recovery in rehabilitation programs through the synchronization of training sessions with sleep.

neuroscience↗