Biology subjects

Della-Maggiore, V.

Publications and source records attributed to Della-Maggiore, V..

8 recordsLinked to original sources

bioRxiv2025

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↗

bioRxiv2024

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.

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bioRxiv2023

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.

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bioRxiv2021

Visuomotor adaptation modulates the clustering of sleep spindles into trains

Sleep spindles are thought to promote memory consolidation. Recently, we have shown that visuomotor adaptation (VMA) learning increases the density of spindles and promotes the coupling between spindles and slow oscillations, locally, with the level of spindle-SO synchrony predicting overnight memory retention. Yet, growing evidence suggests that the rhythmicity in spindle occurrence may also influence the stabilization of declarative and procedural memories. Here, we examined if VMA learning promotes the temporal organization of sleep spindles into trains. We found that VMA increased the proportion of spindles and spindle-SO couplings in trains. In agreement with our previous work, this modulation was observed over the contralateral hemisphere to the trained hand, and predicted overnight memory retention. Interestingly, spindles grouped in a cluster showed greater amplitude and duration than isolated spindles. The fact that these features increased as a function of train length, provides evidence supporting a biological advantage of this temporal arrangement. Our work opens the possibility that the periodicity of NREM oscillations may be relevant in the stabilization of procedural memories. CONTRIBUTION STATEMENTEver since the discovery of memory systems, the study of the mechanisms supporting the consolidation of declarative and procedural memories has progressed somewhat in parallel. We now know, however, that structures originally thought of as purely declarative such as the hippocampus, participate in the consolidation of procedural tasks. Recently, we showed that sleep predicts long-term motor memory through the local synchrony between fast sleep spindles and slow oscillations, a mechanism initially described for the consolidation of declarative memories. Novel evidence has linked the rhythmicity in the occurrence of spindles to memory stabilization. This framework proposes that temporally clustered spindles into trains of two or more separated by 3-6 seconds, may favor the reinstatement and subsequent reprocessing of previously acquired memories. This temporal arrangement may facilitate mnemonic replay and neocortical integration. In the present study, we show that motor learning promotes the organization of spindles into trains, locally, over the contralateral hemisphere, and that this modulation predicts overnight memory retention. Spindle grouping also augmented the proportion of spindle-SO couplings in trains. Importantly, spindles in a cluster increased their duration and amplitude as a function of train length, pointing to a physiological benefit of this temporal organization.

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bioRxiv2020

Competition between parallel sensorimotor learning systems

Sensorimotor adaptation benefits from learning in two parallel systems: one that has access to explicit knowledge, and another that relies on implicit, unconscious correction. However, it is unclear how these systems interact: does enhancing one systems contributions, for example through instruction, impair the other, or do they learn independently? Here we illustrate that certain contexts can lead to competition between implicit and explicit learning. In some cases, each system is responsive to a task-related visual error. This shared error appears to create competition between these systems, such that when the explicit system increases its response, errors are siphoned away from the implicit system, thus reducing its learning. This model suggests that explicit strategy can mask changes in implicit error sensitivity related to savings and interference. Other contexts suggest that the implicit system can respond to multiple error sources. When these error sources conflict, a second type of competition occurs. Thus, the data show that during sensorimotor adaptation, behavior is shaped by competition between parallel learning systems.

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bioRxiv2020

Local coupling between sleep spindles and slow oscillations supports the consolidation of motor memories

Recent studies from us and others suggest that traditionally declarative structures (e.g., hippocampus) mediate some aspects of the encoding and consolidation of procedural memories. This evidence points to the existence of converging physiological pathways across memory systems. Here, we examined whether the coupling between slow oscillations (SO) and spindles, a mechanism well established in the consolidation of declarative memories, is relevant for the stabilization of human motor memories. To this aim, we conducted an EEG study in which we quantified various parameters of these oscillations during a night of sleep that took place immediately after learning a visuomotor adaptation task. We hypothesized that if this coupling is instrumental to motor memory consolidation then spindles locked to the active phase of a slow oscillation would predict long-term memory. We found that visuomotor adaptation increased the overall density of fast ([≥]12 Hz) but not slow (<12Hz) spindles during NREM3. This modulation was manifested rather locally, over the hemisphere contralateral to the trained hand. Although motor learning did not affect the density of SOs, it substantially enhanced the number of fast spindles locked to the active phase of SOs. The fact that only coupled spindles of the left hemisphere predicted long-term memory overnight, points to the precise phase relationship between these oscillations as a fundamental signature of motor memory consolidation. Our work provides evidence in favor of a common mechanism at the basis of the stabilization of declarative and non-declarative memories. Significance StatementEver since the discovery of memory systems, the study of the mechanisms supporting the consolidation of declarative and procedural memories has progressed somewhat in parallel. In the last few years, however, this framework is starting to change. We now know that structures originally thought of as purely declarative, such as the hippocampus, participate in the consolidation of procedural tasks. Here, we show that sleep modulates the stabilization of motor memories through a mechanism involved in the consolidation of declarative memories, based on the local synchrony between fast sleep spindles and slow oscillations. The fact that only coupled -but not uncoupled- spindles of the contralateral hemisphere predicted long-term memory supports a role of this association in the consolidation of motor memories.

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bioRxiv2019

The origins of anterograde interference in visuomotor adaptation

Anterograde interference refers to the negative impact of prior learning on the propensity for future learning. Previous work has shown that subsequent adaptation to two perturbations of opposing sign, A and B, impairs performance in B. Here, we aimed to unveil the mechanism at the basis of anterograde interference by tracking its impact as a function of time through a 24h period. We found that the memory of A biased performance in B for all time intervals. Conversely, learning from error was hindered up to 1h following acquisition of A, with release from interference occurring at 6h. These findings suggest that poor performance induced by prior learning is driven by two distinct mechanisms: a long-lasting bias that acts as a prior and hinders the initial level of performance, and a short-lasting learning impairment that originates from a reduction in error-sensitivity. Our work provides insight into the timeline of memory stabilization in visuomotor adaptation.

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bioRxiv2019

Improving spatial normalization of brain diffusion MRI to measure longitudinal changes of tissue microstructure in human cortex and white matter.

BackgroundFractional anisotropy (FA) and mean diffusivity (MD) are frequently used to evaluate longitudinal changes in white matter microstructure. Recently, there has been a growing interest in identifying experience-dependent plasticity in gray matter using MD. Improving registration has thus become a major goal to enhance the detection of subtle longitudinal changes in cortical microstructure. PurposeTo optimize normalization to improve registration in gray matter and reduce variability associated with multi-session registrations. Study TypeProspective longitudinal study SubjectsTwenty-one healthy subjects (18-31 years old) underwent 9 magnetic resonance imaging (MRI) scanning sessions each. Field Strength/Sequence3.0T, diffusion-weighted multiband-accelerated sequence, MP2RAGE sequence. AssessmentDiffusion-weighted images were registered to standard space using different pipelines that varied in the features used for normalization, namely the non-linear registration algorithm (FSL vs ANTs), the registration target (FA-based vs T1-based templates), and the use of intermediate individual (FA-based or T1-based) targets. We compared the across-session test-retest reproducibility error from these normalization approaches for FA and MD in white and gray matters. Statistical TestsReproducibility errors were compared using a repeated-measures analysis of variance with pipeline as within-subject factor. ResultsThe registration of FA data to the FMRIB58 FA atlas using ANTs yielded lower reproducibility errors in white matter (p<0.0001) with respect to FSL. Moreover, using the MNI152 T1 template as the target of registration resulted in lower reproducibility errors for MD (p<0.0001), whereas the FMRIB58 FA template performed better for FA (p<0.0001). Finally, the use of an intermediate individual template improved reproducibility when registration of the FA images to the MNI152-T1 was carried out within modality (FA-FA) (p<0.05), but not via a T1-based individual template. Data ConclusionA normalization approach using ANTs to register FA images to the MNI152 T1 template via an individual FA template minimized test-retest reproducibility errors both for gray and white matter.

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