RESUMO
In the search for the function of mirror neurons, a previous study reported that F5 mirror neuron responses are modulated by the value that the observing monkey associates with the grasped object. Yet we do not know whether mirror neurons are modulated by the expected reward value for the observer or also by other variables, which are causally dependent on value (e.g., motivation, attention directed at the observed action, arousal). To clarify this, we trained two rhesus macaques to observe a grasping action on an object kept constant, followed by four fully predictable outcomes of different values (2 outcomes with positive and 2 with negative emotional valence). We found a consistent order in population activity of both mirror and nonmirror neurons that matches the order of the value of this predicted outcome but that does not match the order of the above-mentioned value-dependent variables. These variables were inferred from the probability not to abort a trial, saccade latency, modulation of eye position during action observation, heart rate, and pupil size. Moreover, we found subpopulations of neurons tuned to each of the four predicted outcome values. Multidimensional scaling revealed equal normalized distances of 0.25 between the two positive and between the two negative outcomes suggesting the representation of a relative value, scaled to the task setting. We conclude that F5 mirror neurons and nonmirror neurons represent the observer's predicted outcome value, which in the case of mirror neurons may be transferred to the observed object or action.NEW & NOTEWORTHY Both the populations of F5 mirror neurons and nonmirror neurons represent the predicted value of an outcome resulting from the observation of a grasping action. Value-dependent motivation, arousal, and attention directed at the observed action do not provide a better explanation for this representation. The population activity's metric suggests an optimal scaling of value representation to task setting.
Assuntos
Antecipação Psicológica/fisiologia , Memória de Curto Prazo/fisiologia , Neurônios-Espelho/fisiologia , Motivação/fisiologia , Atividade Motora/fisiologia , Córtex Motor/fisiologia , Recompensa , Percepção Visual/fisiologia , Potenciais de Ação/fisiologia , Animais , Atenção/fisiologia , Comportamento Animal/fisiologia , Movimentos Oculares/fisiologia , Tecnologia de Rastreamento Ocular , Humanos , Macaca mulatta , MasculinoRESUMO
Dynamic modulations of large-scale network activity and synchronization are inherent to a broad spectrum of cognitive processes and are disturbed in neuropsychiatric conditions including Parkinson's disease. Here, we set out to address the motor network activity and synchronization in Parkinson's disease and its modulation with subthalamic stimulation. To this end, 20 patients with idiopathic Parkinson's disease with subthalamic nucleus stimulation were analysed on externally cued right hand finger movements with 1.5-s interstimulus interval. Simultaneous recordings were obtained from electromyography on antagonistic muscles (right flexor digitorum and extensor digitorum) together with 64-channel electroencephalography. Time-frequency event-related spectral perturbations were assessed to determine cortical and muscular activity. Next, cross-spectra in the time-frequency domain were analysed to explore the cortico-cortical synchronization. The time-frequency modulations enabled us to select a time-frequency range relevant for motor processing. On these time-frequency windows, we developed an extension of the phase synchronization index to quantify the global cortico-cortical synchronization and to obtain topographic differentiations of distinct electrode sites with respect to their contributions to the global phase synchronization index. The spectral measures were used to predict clinical and reaction time outcome using regression analysis. We found that movement-related desynchronization of cortical activity in the upper alpha and beta range was significantly facilitated with 'stimulation on' compared to 'stimulation off' on electrodes over the bilateral parietal, sensorimotor, premotor, supplementary-motor, and prefrontal areas, including the bilateral inferior prefrontal areas. These spectral modulations enabled us to predict both clinical and reaction time improvement from subthalamic stimulation. With 'stimulation on', interhemispheric cortico-cortical coherence in the beta band was significantly attenuated over the bilateral sensorimotor areas. Similarly, the global cortico-cortical phase synchronization was attenuated, and the topographic differentiation revealed stronger desynchronization over the (ipsilateral) right-hemispheric prefrontal, premotor and sensorimotor areas compared to 'stimulation off'. We further demonstrated that the cortico-cortical phase synchronization was largely dominated by genuine neuronal coupling. The clinical improvement with 'stimulation on' compared to 'stimulation off' could be predicted from this cortical decoupling with multiple regressions, and the reduction of synchronization over the right prefrontal area showed a linear univariate correlation with clinical improvement. Our study demonstrates wide-spread activity and synchronization modulations of the cortical motor network, and highlights subthalamic stimulation as a network-modulating therapy. Accordingly, subthalamic stimulation may release bilateral cortical computational resources by facilitating movement-related desynchronization. Moreover, the subthalamic nucleus is critical to balance inhibitory and facilitatory cortical players within the motor program.
Assuntos
Sincronização Cortical/fisiologia , Estimulação Encefálica Profunda/métodos , Córtex Motor/fisiopatologia , Vias Neurais/fisiopatologia , Doença de Parkinson/terapia , Subtálamo/fisiologia , Adulto , Idoso , Antiparkinsonianos/uso terapêutico , Sincronização Cortical/efeitos dos fármacos , Potencial Evocado Motor/fisiologia , Feminino , Humanos , Levodopa/uso terapêutico , Estudos Longitudinais , Masculino , Pessoa de Meia-Idade , Rede Nervosa/fisiopatologia , Doença de Parkinson/patologia , Desempenho Psicomotor/efeitos dos fármacos , Fatores de Tempo , Resultado do TratamentoRESUMO
According to the mirror mechanism the discharge of F5 mirror neurons of a monkey observing another individual performing an action is a motor representation of the observed action that may serve to understand or learn from the action. This hypothesis, if strictly interpreted, requires mirror neurons to exhibit an action tuning that is shared between action observation and execution. Due to insufficient data it remains contentious if this requirement is met. To fill in the gaps, we conducted an experiment in which identical objects had to be manipulated in three different ways in order to serve distinct action goals. Using three methods, including cross-task classification, we found that at most time points F5 mirror neurons did not encode observed actions with the same code underlying action execution. However, in about 20% of neurons there were time periods with a shared code. These time periods formed a distinct cluster and cannot be considered a product of chance. Population classification yielded non-shared coding for observed actions in the whole population, which was at times optimal and consistently better than shared coding in differentially selected subpopulations. These results support the hypothesis of a representation of observed actions based on a strictly defined mirror mechanism only for small subsets of neurons and only under the assumption of time-resolved readout. Considering alternative concepts and recent findings, we propose that during observation mirror neurons represent the process of a goal pursuit from the observer's viewpoint. Whether the observer's goal pursuit, in which the other's action goal becomes the observer's action goal, or the other's goal pursuit is represented remains to be clarified. In any case, it may allow the observer to use expectations associated with a goal pursuit to directly intervene in or learn from another's action.
Assuntos
Neurônios-Espelho , Córtex Motor , Animais , Macaca , Neurônios-Espelho/fisiologia , Desempenho Psicomotor/fisiologia , Córtex Motor/fisiologia , Potenciais de Ação/fisiologiaRESUMO
Conventional subthalamic deep brain stimulation for Parkinson's disease (PD) presumably modulates the spatial component of gait. However, temporal dysregulation of gait is one of the factors that is tightly associated with freezing of gait (FOG). Temporal locomotor integration may be modulated differentially at distinct levels of the basal ganglia. Owing to its specific descending brainstem projections, stimulation of the substantia nigra pars reticulata (SNr) area might modulate spatial and temporal parameters of gait differentially compared to standard subthalamic nucleus (STN) stimulation. Here, we aimed to characterize the differential effect of STN or SNr stimulation on kinematic gait parameters. We analyzed biomechanical parameters during unconstrained over ground walking in 12 PD patients with subthalamic deep brain stimulation and FOG. Patients performed walking in three therapeutic conditions: (i) Off stimulation, (ii) STN stimulation (alone), and (iii) SNr stimulation (alone). SNr stimulation was achieved by stimulating the most caudal contact of the electrode. We recorded gait using three sensors (each containing a tri-axial accelerometer, gyroscope, and magnetometer) attached on both left and right ankle, and to the lumbar spine. STN stimulation improved both the spatial features (stride length, stride length variability) and the temporal parameters of gait. SNr stimulation improved temporal parameters of gait (swing time asymmetry). Correlation analysis suggested that patients with more medial localization of the SNr contact associated with a stronger regularization of gait. These results suggest that SNr stimulation might support temporal regularization of gait integration.
RESUMO
The purpose of blinks is to keep the eyes hydrated and to protect them. Blinks are rarely noticed by the subject as blink-induced alterations of visual input are blanked out without jeopardizing the perception of visual continuity, features blinks share with saccades. Although not perceived, the blink-induced disconnection from the visual environment leads to a loss of information. Therefore there is critical need to minimize it. Here we demonstrate evidence for a new type of eye movement serving a distinct oculomotor demand, namely the resetting of eye torsion, likewise inevitably causing a loss of visual information. By integrating this eye movement into blinks, the inevitable down times of vision associated with each of the two behaviors are synchronized and the overall downtime minimized.
Assuntos
Piscadela , Movimentos Oculares , Neurônios Motores/fisiologia , Fenômenos Fisiológicos Oculares , Músculos Oculomotores/fisiologia , Adulto , Feminino , Humanos , Masculino , Visão OcularRESUMO
Most patients suffering from chronic idiopathic dizziness do not present signs of vestibular dysfunction or organic failures of other kinds. Hence, this kind of dizziness is commonly seen as psychogenic in nature, sharing commonalities with specific phobias, panic disorder, and generalized anxiety. A more specific concept put forward by Brandt and Dieterich (1) states that these patients suffer from dizziness because of an inadequate compensation of self-induced sensory stimulation. According to this hypothesis self-motion-induced reafferent visual stimulation is interpreted as motion in the world since a predictive signal reflecting the consequences of self-motion, needed to compensate the reafferent stimulus, is inadequate. While conceptually intriguing, experimental evidence supporting the idea of an inadequate prediction of the sensory consequences of own movements has as yet been lacking. Here we tested this hypothesis by applying it to the perception of background motion induced by smooth pursuit eye movements. As a matter of fact, we found the same mildly undercompensating prediction, responsible for the perception of slight illusory world motion ("Filehne illusion") in the 15 patients tested and their age-matched controls. Likewise, the ability to adapt this prediction to the needs of the visual context was not deteriorated in patients. Finally, we could not find any correlation between measures of the individual severity of dizziness and the ability to predict. In sum, our results do not support the concept of a deviant prediction of self-induced sensory stimulation as cause of chronic idiopathic dizziness.