From movement to action: An EEG study into the emerging sense of agency in early infancy.

Research into the developing sense of agency has traditionally focused on sensitivity to sensorimotor contingencies, but whether this implies the presence of a causal action-effect model has recently been called into question. Here, we investigated whether 3- to 4.5-month-old infants build causal action-effect models by focusing on behavioral and neural measures of violation of expectation. Infants had time to explore the causal link between their movements and audiovisual effects before the action-effect contingency was discontinued. We tested their ability to predict the consequences of their movements and recorded neural (EEG) and movement measures. If infants built a causal action-effect model, we expected to observe their violation of expectation in the form of a mismatch negativity (MMN) in the EEG and an extinction burst in their movement behavior after discontinuing the action-effect contingency. Our findings show that the group of infants who showed an MMN upon cessation of the contingent effect demonstrated a more pronounced limb-specific behavioral extinction burst, indicating a causal action-effect model, compared to the group of infants who did not show an MMN. These findings reveal that, in contrast to previous claims, the sense of agency is only beginning to emerge at this age.

Processing of Prediction Errors in Mentalizing Areas.

When seeing people perform actions, we are able to quickly predict the action's outcomes. These predictions are not solely based on the observed actions themselves but utilize our prior knowledge of others. It has been suggested that observed outcomes that are not in line with these predictions result in prediction errors, which require additional processing to be integrated or updated. However, there is no consensus on whether this is indeed the case for the kind of high-level social-cognitive processes involved in action observation. In this fMRI study, we investigated whether observation of unexpected outcomes causes additional activation in line with the processing of prediction errors and, if so, whether this activation overlaps with activation in brain areas typically associated with social-cognitive processes. In the first part of the experiment, participants watched animated movies of two people playing a bowling game, one experienced and one novice player. In cases where the player's score was higher or lower than expected based on their skill level, there was increased BOLD activity in areas that were also activated during a theory of mind task that participants performed in the second part of the experiment. These findings are discussed in the light of different theoretical accounts of human social-cognitive processing.

Cortical volume and sex influence visual gamma.

Visually induced gamma-band activity (GBA) has been implicated in several central cognitive functions, in particular perceptual binding, the feedforward routing of attended stimulus information and memory encoding. Several studies have documented that the strength and frequency of GBA are influenced by both subject-intrinsic factors like age, and subject-extrinsic factors such as stimulus contrast. Here, we investigated the relative contributions of previously tested factors, additional factors, and their interactions, in a cohort of 158 subjects recorded with magnetoencephalography (MEG). In agreement with previous studies, we found that gamma strength and gamma peak frequency increase with stimulus contrast and stimulus velocity. Also in confirmation of previous findings, we report that gamma peak frequency declines with subject age. In addition, we found that gamma peak frequency is higher for subjects with thicker occipital cortex, but lower for larger occipital cortices. Also, gamma peak frequency is higher in female than male subjects. Extrinsic factors (stimulus contrast and velocity) and intrinsic factors (age, cortical thickness and sex) together explained 21% of the variance in gamma peak frequency and 20% of the variance in gamma strength. These results can contribute to our understanding of the mechanisms, by which gamma is generated, and the mechanisms, through which it affects the cognitive performance of a given individual subject.

One wouldn't expect an expert bowler to hit only two pins: Hierarchical predictive processing of agent-caused events.

Evidence is accumulating that our brains process incoming information using top-down predictions. If lower level representations are correctly predicted by higher level representations, this enhances processing. However, if they are incorrectly predicted, additional processing is required at higher levels to "explain away" prediction errors. Here, we explored the potential nature of the models generating such predictions. More specifically, we investigated whether a predictive processing model with a hierarchical structure and causal relations between its levels is able to account for the processing of agent-caused events. In Experiment 1, participants watched animated movies of "experienced" and "novice" bowlers. The results are in line with the idea that prediction errors at a lower level of the hierarchy (i.e., the outcome of how many pins fell down) slow down reporting of information at a higher level (i.e., which agent was throwing the ball). Experiments 2 and 3 suggest that this effect is specific to situations in which the predictor is causally related to the outcome. Overall, the study supports the idea that a hierarchical predictive processing model can account for the processing of observed action outcomes and that the predictions involved are specific to cases where action outcomes can be predicted based on causal knowledge.

Beta- and gamma-band activity reflect predictive coding in the processing of causal events.

In daily life, complex events are perceived in a causal manner, suggesting that the brain relies on predictive processes to model them. Within predictive coding theory, oscillatory beta-band activity has been linked to top-down predictive signals and gamma-band activity to bottom-up prediction errors. However, neurocognitive evidence for predictive coding outside lower-level sensory areas is scarce. We used magnetoencephalography to investigate neural activity during probability-dependent action perception in three areas pivotal for causal inference, superior temporal sulcus, temporoparietal junction and medial prefrontal cortex, using bowling action animations. Within this network, Granger-causal connectivity in the beta-band was found to be strongest for backward top-down connections and gamma for feed-forward bottom-up connections. Moreover, beta-band power in TPJ increased parametrically with the predictability of the action kinematics-outcome sequences. Conversely, gamma-band power in TPJ and MPFC increased with prediction error. These findings suggest that the brain utilizes predictive-coding-like computations for higher-order cognition such as perception of causal events.

Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas.

Primate visual cortex is hierarchically organized. Bottom-up and top-down influences are exerted through distinct frequency channels, as was recently revealed in macaques by correlating inter-areal influences with laminar anatomical projection patterns. Because this anatomical data cannot be obtained in human subjects, we selected seven homologous macaque and human visual areas, and we correlated the macaque laminar projection patterns to human inter-areal directed influences as measured with magnetoencephalography. We show that influences along feedforward projections predominate in the gamma band, whereas influences along feedback projections predominate in the alpha-beta band. Rhythmic inter-areal influences constrain a functional hierarchy of the seven homologous human visual areas that is in close agreement with the respective macaque anatomical hierarchy. Rhythmic influences allow an extension of the hierarchy to 26 human visual areas including uniquely human brain areas. Hierarchical levels of ventral- and dorsal-stream visual areas are differentially affected by inter-areal influences in the alpha-beta band.

Distributed Attention Is Implemented through Theta-Rhythmic Gamma Modulation.

When subjects monitor a single location, visual target detection depends on the pre-target phase of an ∼8 Hz brain rhythm. When multiple locations are monitored, performance decrements suggest a division of the 8 Hz rhythm over the number of locations, indicating that different locations are sequentially sampled. Indeed, when subjects monitor two locations, performance benefits alternate at a 4 Hz rhythm. These performance alternations were revealed after a reset of attention to one location. Although resets are common and important events for attention, it is unknown whether, in the absence of resets, ongoing attention samples stimuli in alternation. Here, we examined whether spatially specific attentional sampling can be revealed by ongoing pre-target brain rhythms. Visually induced gamma-band activity plays a role in spatial attention. Therefore, we hypothesized that performance on two simultaneously monitored stimuli can be predicted by a 4 Hz modulation of gamma-band activity. Brain rhythms were assessed with magnetoencephalography (MEG) while subjects monitored bilateral grating stimuli for a unilateral target event. The corresponding contralateral gamma-band responses were subtracted from each other to isolate spatially selective, target-related fluctuations. The resulting lateralized gamma-band activity (LGA) showed opposite pre-target 4 Hz phases for detected versus missed targets. The 4 Hz phase of pre-target LGA accounted for a 14.5% modulation in performance. These findings suggest that spatial attention is a theta-rhythmic sampling process that is continuously ongoing, with each sampling cycle being implemented through gamma-band synchrony.

Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations.

Neural oscillations have emerged as one of the major electrophysiological phenomena investigated in cognitive and systems neuroscience. These oscillations are typically studied with regard to their amplitude, phase, and/or phase coupling. Here we demonstrate the existence of another property that is intrinsic to neural oscillations but has hitherto remained largely unexplored in cognitive and systems neuroscience. This pertains to the notion that these oscillations show reliable diversity in their phase-relations between neighboring recording sites (phase-relation diversity). In contrast to most previous work, we demonstrate that this diversity is restricted neither to low-frequency oscillations nor to periods outside of sensory stimulation. On the basis of magnetoencephalographic (MEG) recordings in humans, we show that this diversity is prominent not only for ongoing alpha oscillations (8-12 Hz) but also for gamma oscillations (50-70 Hz) that are induced by sustained visual stimulation. We further show that this diversity provides a dimension within electrophysiological data that, provided a sufficiently high signal-to-noise ratio, does not covary with changes in amplitude. These observations place phase-relation diversity on the map as a prominent and general property of neural oscillations that, moreover, can be studied with noninvasive methods in healthy human volunteers. This opens important new avenues for investigating how neural oscillations contribute to the neural implementation of cognition and behavior.

Higher-level processes in the formation and application of associations during action understanding.

The associative account described in the target article provides a viable explanation for the origin of mirror neurons. We argue here that if mirror neurons develop purely by associative learning, then they cannot by themselves explain intentional action understanding. Higher-level processes seem to be involved in the formation of associations as well as in their application during action understanding.

Visual stimulus eccentricity affects human gamma peak frequency.

The peak frequency of neuronal gamma-band synchronization has received much attention in recent years. Gamma peak frequency shifts to higher frequency values for higher contrast, faster moving, and attended stimuli. In monkey V1, gamma peak frequency for a drifting grating is higher for a parafoveal as compared to an eccentric stimulus (Lima et al., 2010). This effect might be due to the cortical magnification factor: the higher cortical magnification for parafoveal stimuli increases the velocity with which the cortical representations of the moving grating stripes move across the cortical surface. Since faster moving stimuli lead to higher gamma frequency, a faster moving cortical representation might do the same. This explanation predicts that the eccentricity effect on gamma peak frequency is absent for stationary stimuli. To test this, we investigated the effect of eccentricity on gamma peak frequency by recording magnetoencephalography in human subjects while they viewed moving or stationary gratings. We found that both the moving and the stationary stimuli induced lower peak frequencies for larger eccentricities, arguing against an explanation based on the cortical magnification factor. We further investigated whether this eccentricity effect was explained by differences in the size or the spatial frequency of the expected cortical activation. Neither of those explained the eccentricity effect. We propose that the different stimulus and top-down factors leading to higher gamma peak frequency all result in higher stimulus salience, that salience is translated into gamma peak frequency, and that gamma peak frequency might subserve the preferential processing of neuronal activity induced by salient stimuli.

Magnetoencephalography in twins reveals a strong genetic determination of the peak frequency of visually induced γ-band synchronization.

Many aspects of brain processing are intimately linked to brain rhythms. Essentially all classical brain rhythms, i.e., delta, theta, alpha, beta, and sleep waves, are highly heritable. This renders brain rhythms an interesting intermediate phenotype for cognitive and behavioral traits. One brain rhythm that has been particularly strongly linked to cognition is the gamma rhythm: it is involved in attention, short- and long-term memory, and conscious awareness. It has been described in sensory and motor cortices, association and control structures, and the hippocampus. In contrast to most other brain rhythms, the gamma frequency highly depends on stimulus and task conditions, suggesting a low heritability. However, the heritability of gamma has not been assessed. Here, we show that visually induced gamma-band synchronization in humans is strongly genetically determined. Eighty twin subjects (20 monozygotic and 20 dizygotic twin pairs) viewed a moving sinusoidal grating while their brain activity was recorded using magnetoencephalography. The stimulus induced spectrally confined gamma-band activity in sensors over visual cortex in all subjects, with individual peak frequencies ranging from 45 to 85 Hz. Gamma-band peak frequencies were highly correlated across monozygotic twins (r = 0.88), but not across dizygotic twins (r = 0.32) or unrelated subjects (r = 0.02). This implies a heritability of the gamma-band frequency of 91%. This strong genetic determination suggests that gamma-related cognitive functions are under close genetic control.

Repetition suppression dissociates spatial frames of reference in human saccade generation.

The path from perception to action involves the transfer of information across various reference frames. Here we applied a functional magnetic resonance imaging (fMRI) repetition suppression paradigm to determine the reference frame(s) in which the cortical activity is coded at several phases of the sensorimotor transformation for a saccade, including sensory processing, saccade planning, and saccade execution. We distinguished between retinal (eye-centered) and nonretinal (e.g., head-centered) coding frames in three key regions: the intraparietal sulcus (IPS), frontal eye field (FEF), and supplementary eye field (SEF). Subjects (n = 18) made delayed saccades to one of five possible peripheral targets, separated at intervals of 9° visual angle. Target locations were chosen pseudorandomly, based on a 2 × 2 factorial design, with factors retinal and nonretinal coordinates and levels novel and repeated. In all three regions, analysis of the blood oxygenation level dependent dynamics revealed an attenuation of the fMRI signal in trials repeating the location of the target in retinal coordinates. The amount of retinal suppression varied across the three phases of the trial, with the strongest suppression during saccade planning. The paradigm revealed only weak traces of nonretinal coding in these regions. Further analyses showed an orderly representation of the retinal target location, as expressed by a contralateral bias of activation, in the IPS and FEF, but not in the SEF. These results provide evidence that the sensorimotor processing in these centers reflects saccade generation in eye-centered coordinates, irrespective of their topographic organization.

Behavioral and cortical mechanisms for spatial coding and action planning.

There is considerable evidence that the encoding of intended actions in visual space is represented in dynamic, gaze-centered maps, such that each eye movement requires an internal updating of these representations. Here, we review results from our own experiments on human subjects that test the additional geometric constraints to the dynamic updating of these spatial maps during whole-body motion. Subsequently, we summarize evidence and present new analyses of how these spatial signals may be integrated with motor effector signals in order to generate the appropriate commands for action. Finally, we discuss neuroimaging experiments suggesting that the posterior parietal cortex and the dorsal premotor cortex play selective roles in this process.

Updating target distance across eye movements in depth.

We tested between two coding mechanisms that the brain may use to retain distance information about a target for a reaching movement across vergence eye movements. If the brain was to encode a retinal disparity representation (retinal model), i.e., target depth relative to the plane of fixation, each vergence eye movement would require an active update of this representation to preserve depth constancy. Alternatively, if the brain was to store an egocentric distance representation of the target by integrating retinal disparity and vergence signals at the moment of target presentation, this representation should remain stable across subsequent vergence shifts (nonretinal model). We tested between these schemes by measuring errors of human reaching movements (n = 14 subjects) to remembered targets, briefly presented before a vergence eye movement. For comparison, we also tested their directional accuracy across version eye movements. With intervening vergence shifts, the memory-guided reaches showed an error pattern that was based on the new eye position and on the depth of the remembered target relative to that position. This suggests that target depth is recomputed after the gaze shift, supporting the retinal model. Our results also confirm earlier literature showing retinal updating of target direction. Furthermore, regression analyses revealed updating gains close to one for both target depth and direction, suggesting that the errors arise after the updating stage during the subsequent reference frame transformations that are involved in reaching.

Gaze-centered updating of remembered visual space during active whole-body translations.

Various cortical and sub-cortical brain structures update the gaze-centered coordinates of remembered stimuli to maintain an accurate representation of visual space across eyes rotations and to produce suitable motor plans. A major challenge for the computations by these structures is updating across eye translations. When the eyes translate, objects in front of and behind the eyes' fixation point shift in opposite directions on the retina due to motion parallax. It is not known if the brain uses gaze coordinates to compute parallax in the translational updating of remembered space or if it uses gaze-independent coordinates to maintain spatial constancy across translational motion. We tested this by having subjects view targets, flashed in darkness in front of or behind fixation, then translate their body sideways, and subsequently reach to the memorized target. Reach responses showed parallax-sensitive updating errors: errors increased with depth from fixation and reversed in lateral direction for targets presented at opposite depths from fixation. In a series of control experiments, we ruled out possible biasing factors such as the presence of a fixation light during the translation, the eyes accompanying the hand to the target, and the presence of visual feedback about hand position. Quantitative geometrical analysis confirmed that updating errors were better described by using gaze-centered than gaze-independent coordinates. We conclude that spatial updating for translational motion operates in gaze-centered coordinates. Neural network simulations are presented suggesting that the brain relies on ego-velocity signals and stereoscopic depth and direction information in spatial updating during self-motion.

Behavioral reference frames for planning human reaching movements.

At some stage in the process of a sensorimotor transformation for a reaching movement, information about the current position of the hand and information about the location of the target must be encoded in the same frame of reference to compute the hand-to-target difference vector. Two main hypotheses have been proposed regarding this reference frame: an eye-centered and a body-centered frame. Here we evaluated these hypotheses using the pointing errors that subjects made when planning and executing arm movements to memorized targets starting from various initial hand positions while keeping gaze fixed in various directions. One group of subjects (n = 10) was tested without visual information about hand position during movement planning (unseen-hand condition); another group (n = 8) was tested with hand and target position simultaneously visible before movement onset (seen-hand condition). We found that both initial hand position and gaze fixation direction had a significant effect on the magnitude and direction of the pointing error. Errors were significantly smaller in the seen-hand condition. For both conditions, though, a reference frame analysis showed that the errors arose at an eye- or hand-centered stage or both, but not at a body-centered stage. As a common reference frame is required to specify a movement vector, these results suggest that an eye-centered mechanism is involved in integrating target and hand position in programming reaching movements. We discuss how simple gain elements modulating the eye-centered target and hand-position signals can account for these results.