ABSTRACT
Targeted memory reactivation (TMR) during sleep enhances memory consolidation in young adults by modulating electrophysiological markers of neuroplasticity. Interestingly, older adults exhibit deficits in motor memory consolidation, an impairment that has been linked to age-related degradations in the same sleep features sensitive to TMR. We hypothesised that TMR would enhance consolidation in older adults via the modulation of these markers. A total of 17 older participants were trained on a motor task involving two auditory-cued sequences. During a post-learning nap, two auditory cues were played: one associated to a learned (i.e., reactivated) sequence and one control. Performance during two delayed re-tests did not differ between reactivated and non-reactivated sequences. Moreover, both associated and control sounds modulated brain responses, yet there were no consistent differences between the auditory cue types. Our results collectively demonstrate that older adults do not benefit from specific reactivation of a motor memory trace by an associated auditory cue during post-learning sleep. Based on previous research, it is possible that auditory stimulation during post-learning sleep could have boosted motor memory consolidation in a non-specific manner.
Subject(s)
Memory Consolidation , Memory , Young Adult , Humans , Aged , Memory/physiology , Memory Consolidation/physiology , Learning/physiology , Sleep/physiology , CuesABSTRACT
Previous behavioral, clinical, and neuroimaging studies suggest that the neural substrates of adaptation of saccadic eye movements involve, beyond the central role of the cerebellum, several, still incompletely determined, cortical areas. Furthermore, no neuroimaging study has yet tackled the differences between saccade lengthening ("forward adaptation") and shortening ("backward adaptation") and neither between their two main components, i.e. error processing and oculomotor changes. The present fMRI study was designed to fill these gaps. Blood-oxygen-level-dependent (BOLD) signal and eye movements of 24 healthy volunteers were acquired while performing reactive saccades under 4 conditions repeated in short blocks of 16 trials: systematic target jump during the saccade and in the saccade direction (forward: FW) or in the opposite direction (backward: BW), randomly directed FW or BW target jump during the saccade (random: RND) and no intra-saccadic target jump (stationary: STA). BOLD signals were analyzed both through general linear model (GLM) approaches applied at the whole-brain level and through sensitive Multi-Variate Pattern Analyses (MVPA) applied to 34 regions of interest (ROIs) identified from independent 'Saccade Localizer' functional data. Oculomotor data were consistent with successful induction of forward and backward adaptation in FW and BW blocks, respectively. The different analyses of voxel activation patterns (MVPAs) disclosed the involvement of 1) a set of ROIs specifically related to adaptation in the right occipital cortex, right and left MT/MST, right FEF and right pallidum; 2) several ROIs specifically involved in error signal processing in the left occipital cortex, left PEF, left precuneus, Medial Cingulate cortex (MCC), left inferior and right superior cerebellum; 3) ROIs specific to the direction of adaptation in the occipital cortex and MT/MST (left and right hemispheres for FW and BW, respectively) and in the pallidum of the right hemisphere (FW). The involvement of the left PEF and of the (left and right) occipital cortex were further supported and qualified by the whole brain GLM analysis: clusters of increased activity were found in PEF for the RND versus STA contrast (related to error processing) and in the left (right) occipital cortex for the FW (BW) versus STA contrasts [related to the FW (BW) direction of error and/or adaptation]. The present study both adds complementary data to the growing literature supporting a role of the cerebral cortex in saccadic adaptation through feedback and feedforward relationships with the cerebellum and provides the basis for improving conceptual frameworks of oculomotor plasticity and of its link with spatial cognition.
Subject(s)
Neuronal Plasticity , Saccades , Adaptation, Physiological/physiology , Brain Mapping , Cerebellum/physiology , Humans , Magnetic Resonance Imaging , PlasticsABSTRACT
Attention and saccadic adaptation (SA) are critical components of visual perception, the former enhancing sensory processing of selected objects, the latter maintaining the eye movements accuracy toward them. Recent studies propelled the hypothesis of a tight functional coupling between these mechanisms, possibly due to shared neural substrates. Here, we used magnetoencephalography to investigate for the first time the neurophysiological bases of this coupling and of SA per se. We compared visual discrimination performance of 12 healthy subjects before and after SA. Eye movements and magnetic signals were recorded continuously. Analyses focused on gamma band activity (GBA) during the pretarget period of the discrimination and the saccadic tasks. We found that GBA increases after SA. This increase was found in the right hemisphere for both postadaptation saccadic and discrimination tasks. For the latter, GBA also increased in the left hemisphere. We conclude that oculomotor plasticity involves GBA modulation within an extended neural network which persists after SA, suggesting a possible role of gamma oscillations in the coupling between SA and attention.
Subject(s)
Adaptation, Physiological , Attention/physiology , Brain/physiology , Gamma Rhythm , Psychomotor Performance/physiology , Saccades , Visual Perception/physiology , Adult , Discrimination, Psychological/physiology , Eye Movement Measurements , Female , Humans , Magnetoencephalography , MaleABSTRACT
Targeted memory reactivation (TMR) during post-learning sleep is known to enhance motor memory consolidation but the underlying neurophysiological processes remain unclear. Here, we confirm the beneficial effect of auditory TMR on motor performance. At the neural level, TMR enhanced slow wave (SW) characteristics. Additionally, greater TMR-related phase-amplitude coupling between slow (0.5-2 Hz) and sigma (12-16 Hz) oscillations after the SW peak was related to higher TMR effect on performance. Importantly, sounds that were not associated to learning strengthened SW-sigma coupling at the SW trough. Moreover, the increase in sigma power nested in the trough of the potential evoked by the unassociated sounds was related to the TMR benefit. Altogether, our data suggest that, depending on their precise temporal coordination during post learning sleep, slow and sigma oscillations play a crucial role in either memory reinstatement or protection against irrelevant information; two processes that critically contribute to motor memory consolidation.
Subject(s)
Memory Consolidation , Electroencephalography , Learning/physiology , Memory Consolidation/physiology , Sleep/physiology , SoundABSTRACT
Attention and saccadic eye movements are critical components of visual perception. Recent studies proposed the hypothesis of a tight coupling between saccadic adaptation (SA) and attention: SA increases the processing speed of unpredictable stimuli, while increased attentional load boosts SA. Moreover, their cortical substrates partially overlap. Here, we investigated for the first time whether this coupling in the reactive/exogenous modality is specific to the orienting system of attention. We studied the effect of adaptation of reactive saccades (RS), elicited by the double-step paradigm, on exogenous orienting, measured using a Posner-like detection paradigm. In 18 healthy subjects, the attentional benefit-the difference in reaction time to targets preceded by informative versus uninformative cues-in a control exposure condition was subtracted from that of each adaptation exposure condition (backward and forward); then, this cue benefit difference was compared between the pre- and post-exposure phases. We found that, the attentional benefit significantly increased for cued-targets presented in the left hemifield after backward adaptation and for cued-targets presented in the right hemifield after forward adaptation. These findings provide strong evidence in humans for a coupling between RS adaptation and attention, possibly through the activation of a common neuronal pool.
Subject(s)
Attention/physiology , Orientation, Spatial/physiology , Saccades/physiology , Adaptation, Physiological , Adult , Cues , Female , Healthy Volunteers , Humans , Male , Orientation/physiology , Photic Stimulation/methods , Reaction Time/physiology , Visual Perception/physiologyABSTRACT
To what extent oculomotor and attention systems are linked remains strongly debated. Previous studies suggested that saccadic adaptation, a well-studied model of oculomotor plasticity, and orienting of attention rely on overlapping networks in the parietal cortex and can functionally interact. Using a Posner-like paradigm in healthy human subjects, we demonstrate for the first time that saccadic adaptation boosts endogenous attention orienting. Indeed, the discrimination of perifoveal targets benefits more from central cues after backward adaptation of leftward voluntary saccades than after a control saccade task. We propose that the overlap of underlying neural networks actually consists of neuronal populations co-activated by oculomotor plasticity and endogenous attention deployed perifoveally. The functional coupling demonstrated here plaids for conceptual models not belonging to the framework of the premotor theory of attention as the latter has been rejected precisely for this voluntary/endogenous modality. These results also open new perspective for rehabilitation of visuo-attentional deficits.
Subject(s)
Attention , Orientation , Saccades , Adult , Female , Humans , Male , Nerve Net/physiology , Parietal Lobe/physiology , Visual Perception , Young AdultABSTRACT
Stereopsis - 3D vision - has become widely used as a model of perception. However, all our knowledge of possible underlying mechanisms comes almost exclusively from vertebrates. While stereopsis has been demonstrated for one invertebrate, the praying mantis, a lack of techniques to probe invertebrate stereopsis has prevented any further progress for three decades. We therefore developed a stereoscopic display system for insects, using miniature 3D glasses to present separate images to each eye, and tested our ability to deliver stereoscopic illusions to praying mantises. We find that while filtering by circular polarization failed due to excessive crosstalk, "anaglyph" filtering by spectral content clearly succeeded in giving the mantis the illusion of 3D depth. We thus definitively demonstrate stereopsis in mantises and also demonstrate that the anaglyph technique can be effectively used to deliver virtual 3D stimuli to insects. This method opens up broad avenues of research into the parallel evolution of stereoscopic computations and possible new algorithms for depth perception.
Subject(s)
Depth Perception , Insecta , Visual Perception , AnimalsABSTRACT
PURPOSE: Visual exploration relies on saccadic eye movements and attention processes. Saccadic adaptation mechanisms, which calibrate the oculomotor commands to continuously maintain the accuracy of saccades, have been suggested to act at downstream (motor) and upstream (visuoattentional) levels of visuomotor transformation. Conversely, whether attention can directly affect saccadic adaptation remains unknown. To answer this question, we manipulated the level of attention engaged in a visual discrimination task performed during saccadic adaptation. METHODS: Participants performed low or high attention demanding orientation discrimination tasks on largely or faintly oriented Gabor patches, respectively, which served as targets for reactive saccades. Gabor patches systematically jumped backward during eye motion to elicit an adaptive shortening of saccades, and replaced 50 msec later (100 msec in two subjects) by a mask. Subjects judged whether Gabors' orientation was "nearly horizontal" versus "nearly vertical" (low attention demanding) or "slightly left" versus "slightly right" (high attention demanding), or made no discrimination (control task). RESULTS: We found that the build-up and the retention of adaptation of reactive saccades were larger in the "high attention demanding" condition than in the "low attention demanding" and the no-discrimination control conditions. CONCLUSIONS: These results indicate that increasing the level of attention to the perceptual processing of otherwise identical targets boosts saccadic adaptation, and suggest that saccadic adaptation mechanisms and attentional load effects may functionally share common neural substrates.