RESUMEN
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.
Asunto(s)
Anticipación Psicológica/fisiología , Memoria a Corto Plazo/fisiología , Neuronas Espejo/fisiología , Motivación/fisiología , Actividad Motora/fisiología , Corteza Motora/fisiología , Recompensa , Percepción Visual/fisiología , Potenciales de Acción/fisiología , Animales , Atención/fisiología , Conducta Animal/fisiología , Movimientos Oculares/fisiología , Tecnología de Seguimiento Ocular , Humanos , Macaca mulatta , MasculinoRESUMEN
Blinks do not only protect the eye, but they do also correct for torsional eye position deviations by blink-associated resetting eye movements (BARMs). Although BARMs are functionally distinct from other eye movements in the torsional dimension, it has remained open if BARMs observed in the horizontal and vertical dimensions (fixational BARMs) are not simply microsaccades coinciding with blinks. We show here that fixational BARMs are functionally distinct and complementary to microsaccades in the following way: First, they compensate for large fixational error more efficiently than microsaccades, secondly, their probability to be executed in eccentric eye positions is higher, and thirdly, they reset the eyes into a position zone that is broader as compared to microsaccades. This suggests that BARMs help to keep the eyes in a working range wherein microsaccades guarantee high acuity vision. Moreover, we establish that fixational BARMs operate in a retina-centric frame.
Asunto(s)
Parpadeo , Movimientos Oculares , Movimientos Sacádicos/fisiología , Animales , Fijación Ocular , Macaca mulatta , Masculino , Agudeza VisualRESUMEN
Humans derive causality judgments reliably from highly abstract stimuli, such as moving discs that bump into each other [1]. This fascinating visual capability emerges gradually during human development [2], perhaps as consequence of sensorimotor experience [3]. Human functional imaging studies suggest an involvement of the "action observation network" in the processing of such stimuli [4, 5]. In addition, theoretical studies suggest a link between the computational mechanisms of action and causality perception [6, 7], consistent with the fact that both functions require an analysis of sequences of spatiotemporal relationships between interacting stimulus elements. Single-cell correlates of the perception of causality are completely unknown. In order to find such neural correlates, we investigated the responses of "mirror neurons" in macaque premotor area F5 [8, 9]. These neurons respond during the observation as well as during the execution of actions and show interesting invariances, e.g., with respect to the stimulus view [10], occlusions [11], or whether an action is really executed or suppressed [12]. We investigated the spatiotemporal properties of the visual responses of mirror neurons to naturalistic hand action stimuli and to abstract stimuli, which specified the same causal relationships. We found a high degree of generalization between these two stimulus classes. In addition, many features that strongly reduced the similarity of the response patterns coincided with the ones that also destroy the perception of causality in humans. This implies an overlap of neural structures involved in the processing of actions and the visual perception of causality at the single-cell level.
Asunto(s)
Macaca mulatta/fisiología , Neuronas Espejo/fisiología , Corteza Motora/fisiología , Percepción Visual/fisiología , Animales , Masculino , Estimulación LuminosaRESUMEN
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.
Asunto(s)
Parpadeo , Movimientos Oculares , Neuronas Motoras/fisiología , Fenómenos Fisiológicos Oculares , Músculos Oculomotores/fisiología , Adulto , Femenino , Humanos , Masculino , Visión OcularRESUMEN
Hippocampal specimens resected to cure medically intractable temporal lobe epilepsy (TLE) provide a unique possibility to study functional consequences of morphological alterations. One intriguing alteration predominantly observed in cases of hippocampal sclerosis is an uncommon network of granule cells monosynaptically interconnected via aberrant supragranular mossy fibers. We investigated whether granule cell populations in slices from sclerotic and nonsclerotic hippocampi would develop ictaform activity when challenged by low-frequency hilar stimulation in the presence of elevated extracellular potassium concentration (10 and 12 mm) and whether the experimental activity differs according to the presence of aberrant mossy fibers. We found that ictaform activity could be evoked in slices from sclerotic and nonsclerotic hippocampi (27 of 40 slices, 14 of 20 patients; and 11 of 22 slices, 6 of 12 patients, respectively). However, the two patient groups differed with respect to the pattern of ictaform discharges and the potassium concentration mandatory for its induction. Seizure-like events were already induced with 10 mm K+. They exclusively occurred in slices from sclerotic hippocampi, of which 80% displayed stimulus-induced oscillatory population responses (250-300 Hz). In slices from nonsclerotic hippocampi, atypical negative field potential shifts were predominantly evoked with 12 mm K+. In both groups, the ictaform activity was sensitive to ionotropic glutamate receptor antagonists and lowering of [Ca2+]o. Our results show that, in granule cell populations of hippocampal slices from TLE patients, high K+-induced seizure-like activity and ictal spiking coincide with basic electrophysiological abnormalities, hippocampal sclerosis, and mossy fiber sprouting, suggesting that network reorganization could play a crucial role in determining type and threshold of such activity.
Asunto(s)
Giro Dentado/fisiopatología , Epilepsia del Lóbulo Temporal/fisiopatología , Hipocampo/patología , Potasio/metabolismo , Adulto , Calcio/metabolismo , Electrofisiología , Epilepsia del Lóbulo Temporal/patología , Antagonistas de Aminoácidos Excitadores/farmacología , Líquido Extracelular/metabolismo , Fluorometría , Hipocampo/fisiopatología , Humanos , Técnicas In Vitro , Fibras Musgosas del Hipocampo/patología , Neuronas/patología , Receptores de Glutamato/efectos de los fármacos , Esclerosis , Sinapsis/fisiologíaRESUMEN
Repetitive presentation of the same visual stimulus entails a response decrease in the action potential discharge of neurons in various areas of the monkey visual cortex. It is still unclear whether this repetition suppression effect is also present in single neurons in cortical premotor areas responding to visual stimuli, as suggested by the human functional magnetic resonance imaging literature. Here we report the responses of 'mirror neurons' in monkey area F5 to the repeated presentation of action movies. We find that most single neurons and the population at large do not show a significant decrease of the firing rate. On the other hand, simultaneously recorded local field potentials exhibit repetition suppression. As local field potentials are believed to be better linked to the blood-oxygen-level-dependent (BOLD) signal exploited by functional magnetic resonance imaging, these findings suggest caution when trying to derive conclusions on the spiking activity of neurons in a given area based on the observation of BOLD repetition suppression.
Asunto(s)
Adaptación Ocular/fisiología , Macaca mulatta/fisiología , Neuronas Espejo/fisiología , Percepción Visual/fisiología , Potenciales de Acción/fisiología , Animales , Humanos , Masculino , Estimulación Luminosa , Análisis y Desempeño de Tareas , Factores de TiempoRESUMEN
Converging experimental evidence indicates that mirror neurons in the monkey premotor area F5 encode the goals of observed motor acts [1-3]. However, it is unknown whether they also contribute to encoding the perspective from which the motor acts of others are seen. In order to address this issue, we recorded the visual responses of mirror neurons of monkey area F5 by using a novel experimental paradigm based on the presentation of movies showing grasping motor acts from different visual perspectives. We found that the majority of the tested mirror neurons (74%) exhibited view-dependent activity with responses tuned to specific points of view. A minority of the tested mirror neurons (26%) exhibited view-independent responses. We conclude that view-independent mirror neurons encode action goals irrespective of the details of the observed motor acts, whereas the view-dependent ones might either form an intermediate step in the formation of view independence or contribute to a modulation of view-dependent representations in higher-level visual areas, potentially linking the goals of observed motor acts with their pictorial aspects.