Angelika Lingnau

Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans

Neurons in macaque ventral premotor cortex and inferior parietal lobe discharge during both the observation and the execution of motor acts. It has been claimed that these so-called mirror neurons form the basis of action understanding by matching the visual input with the corresponding motor program (direct matching). Functional magnetic resonance imaging (fMRI) adaptation can be used to test the direct matching account of action recognition by determining whether putative mirror neurons show adaptation for repeated motor acts independently of whether they are observed or executed. An unambiguous test of the hypothesis requires that the motor acts be meaningless to ensure that any adaptation effect is directly because of movement recognition/motor execution and not contextually determined inferences. We found adaptation for motor acts that were repeatedly observed or repeatedly executed. We also found adaptation for motor acts that were first observed and then executed, as would be expected if a previously seen act primed the subsequent execution of that act. Crucially, we found no signs of adaptation for motor acts that were first executed and then observed. Failure to find cross-modal adaptation for executed and observed motor acts is not compatible with the core assumption of mirror neuron theory, which holds that action recognition and understanding are based on motor simulation.

The time course of response inhibition in masked priming.

In two experiments, we studied the temporal dynamics of the response time effects of masked visual prime stimuli, as a function of stimulus eccentricity and size. Experiment 1 factorially varied prime—target congruency, eccentricity, and mask—target stimulus onset asynchrony. Early facilitative and late inhibitory effects of congruency were observed at all eccentricities, with temporal dynamics modulated by eccentricity. To test whether this dependence on eccentricity is due to cortical magnification, Experiment 2 varied stimulus size as well. Response inhibition time courses were influenced by size and eccentricity jointly, with no discernible difference when stimuli were matched for cortical magnification. Analysis of the individual time course data revealed that the timescale of inhibition changes with the strength of the cortical representation of the prime stimulus. This imposes constraints on possible models.

The lateral occipitotemporal cortex in action

Understanding and responding to other peoples actions is fundamental for social interactions. Whereas many studies emphasize the importance of parietal and frontal regions for these abilities, several lines of recent research show that the human lateral occipitotemporal cortex (LOTC) represents varied aspects of action, ranging from perception of tools and bodies and the way they typically move, to understanding the meaning of actions, to performing overt actions. Here, we highlight common themes across these lines of work, which have informed theories related to high-level vision, concepts, social cognition, and apraxia. We propose that patterns of activity in LOTC form representational spaces, the dimensions of which capture perceptual, semantic, and motor knowledge of how actions change the state of the world.

Embodied Cognition and Mirror Neurons: A Critical Assessment

According to embodied cognition theories, higher cognitive abilities depend on the reenactment of sensory and motor representations. In the first part of this review, we critically analyze the central claims of embodied theories and argue that the existing behavioral and neuroimaging data do not allow investigators to discriminate between embodied cognition and classical cognitive accounts, which assume that conceptual representations are amodal and symbolic. In the second part, we review the main claims and the core electrophysiological findings typically cited in support of the mirror neuron theory of action understanding, one of the most influential examples of embodied cognition theories. In the final part, we analyze the claim that mirror neurons subserve action understanding by mapping visual representations of observed actions on motor representations, trying to clarify in what sense the representations carried by these neurons can be claimed motor.

Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation

Many neurons in the macaque visual area MSTd are sensitive to the global structure of a pattern of moving dots, responding to optic flow components such as expansion and rotation. Direct evidence for neurons with similar properties in humans has been lacking. We have explored sensitivity to optic flow in the human occipital cortex using an event‐related functional magnetic resonance imaging adaptation paradigm. On each trial, two brief random‐dot kinematograms were presented sequentially. Attention was controlled with a demanding task at fixation. In human MST, the compound response was smaller (indicating adaptation) when the two had the same flow structure than when they were different, suggesting the presence of separate neural populations sensitive to rotation and expansion. Surprisingly, the middle‐temporal (MT) gyrus visual area also showed signs of flow specificity, and even V3A showed weak specificity. In V1, which is expected to respond only to local dot motions, no evidence of flow‐specific neurons was found. The same was true in V2, V3, V3B and V4. Control experiments showed that the results cannot be attributed to adaptation to local translation within the flow pattern, or to attentional effects. Our results clearly demonstrate selective responses to specific optic flow structures in MST, and we tentatively suggest that the human MT and even V3A may show similar properties.

Decoding actions at different levels of abstraction

Brain regions that mediate action understanding must contain representations that are action specific and at the same time tolerate a wide range of perceptual variance. Whereas progress has been made in understanding such generalization mechanisms in the object domain, the neural mechanisms to conceptualize actions remain unknown. In particular, there is ongoing dissent between motor-centric and cognitive accounts whether premotor cortex or brain regions in closer relation to perceptual systems, i.e., lateral occipitotemporal cortex, contain neural populations with such mapping properties. To date, it is unclear to which degree action-specific representations in these brain regions generalize from concrete action instantiations to abstract action concepts. However, such information would be crucial to differentiate between motor and cognitive theories. Using ROI-based and searchlight-based fMRI multivoxel pattern decoding, we sought brain regions in human cortex that manage the balancing act between specificity and generality. We investigated a concrete level that distinguishes actions based on perceptual features (e.g., opening vs closing a specific bottle), an intermediate level that generalizes across movement kinematics and specific objects involved in the action (e.g., opening different bottles with cork or screw cap), and an abstract level that additionally generalizes across object category (e.g., opening bottles or boxes). We demonstrate that the inferior parietal and occipitotemporal cortex code actions at abstract levels whereas the premotor cortex codes actions at the concrete level only. Hence, occipitotemporal, but not premotor, regions fulfill the necessary criteria for action understanding. This result is compatible with cognitive theories but strongly undermines motor theories of action understanding.

Tuning Curves for Movement Direction in the Human Visuomotor System

Neurons in macaque primary motor cortex (M1) are broadly tuned to arm movement direction. Recent evidence suggests that human M1 contains directionally tuned neurons, but it is unclear which other areas are part of the network coding movement direction and what characterizes the responses of neuronal populations in those areas. Such information would be highly relevant for the implementation of brain–computer interfaces (BCIs) in paralyzed patients. We used functional magnetic resonance imaging adaptation to identify which areas of the human brain show directional selectivity and the degree to which these areas are affected by the type of motor act (to press vs to grasp). After adapting participants to one particular hand movement direction, we measured the release from adaptation during occasional test trials, parametrically varying the angular difference between adaptation and test direction. We identified multiple areas broadly tuned to movement direction, including M1, dorsal premotor cortex, intraparietal sulcus, and the parietal reach region. Within these areas, we observed a gradient of directional selectivity, with highest directional selectivity in the right parietal reach region, for both right- and left-hand movements. Moreover, directional selectivity was modulated by the type of motor act to varying degrees, with the largest effect in M1 and the smallest modulation in the parietal reach region. These data provide an important extension of our knowledge about directional tuning in the human brain. Furthermore, our results suggest that the parietal reach region might be an ideal candidate for the implementation of BCI in paralyzed patients.

Overlapping representations for grip type and reach direction

To grasp an object, we need to move the arm toward it and assume the appropriate hand configuration. While previous studies suggested dorsomedial and dorsolateral pathways in the brain specialized respectively for the transport and grip components, more recent studies cast doubt on such a clear-cut distinction. It is unclear, however, to which degree neuronal populations selective for the two components overlap, and if so, to which degree they interact. Here, we used multivoxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data to investigate the representation of three center-out movements (touch, pincer grip, whole-hand grip) performed in five reach directions. We found selectivity exclusively for reach direction in posterior and rostral superior parietal lobes (SPLp, SPLr), supplementary motor area (SMA), and the superior portion of dorsal premotor cortex (PMDs). Instead, we found selectivity for both grip type and reach direction in the inferior portion of dorsal premotor cortex (PMDi), ventral premotor cortex (PMv), anterior intraparietal sulcus (aIPS), primary motor (M1), somatosensory (S1) cortices and the anterior superior parietal lobe (SPLa). Within these regions, PMv, M1, aIPS and SPLa showed weak interactions between the transport and grip components. Our results suggest that human PMDi and S1 contain both grip- and reach-direction selective neuronal populations that retain their functional independence, whereas this information might be combined at the level of PMv, M1, aIPS, and SPLa.

Speed encoding in human visual cortex revealed by fMRI adaptation

In macaque visual cortex, the conventional view is that image motion is initially detected by direction-sensitive neurons that are tuned in terms of local spatial and temporal frequency (TF), from which speed is encoded later. We used functional magnetic resonance imaging (fMRI) adaptation to seek evidence for speed or TF tuning in human visual cortex. Drifting sine-wave gratings were presented in pairs (S1: adapter, 100% contrast; S2: probe, 15, 40 or 80% contrast). In each trial, either speed or TF was the same for S1 and S2, whereas the other dimension changed. We investigated whether the response was weaker (adapted) for repetitions of the same speed, indicating speed coding, or for repetitions of TF, indicating TF coding. For high-contrast (80%) probes, we observed clear speed coding in MT and MST with similar but weaker trends in several earlier visual areas. For medium- and low contrast probes, our data indicated a trend towards temporal frequency coding in most visual areas studied. In a second experiment, we adjusted stimuli in terms of perceived rather than physical speed and found a trend for speed coding even for low-contrast probes. Our results suggest that speed coding dominates in MT/MST for high contrast stimuli, and possibly also in other visual areas and/or at lower contrasts.

Neural correlates of grasping

Prehension, the capacity to reach and grasp objects, comprises two main components: reaching, i.e., moving the hand towards an object, and grasping, i.e., shaping the hand with respect to its properties. Knowledge of this topic has gained a huge advance in recent years, dramatically changing our view on how prehension is represented within the dorsal stream. While our understanding of the various nodes coding the grasp component is rapidly progressing, little is known of the integration between grasping and reaching. With this Mini Review we aim to provide an up-to-date overview of the recent developments on the coding of prehension. We will start with a description of the regions coding various aspects of grasping in humans and monkeys, delineating where it might be integrated with reaching. To gain insights into the causal role of these nodes in the coding of prehension, we will link this functional description to lesion studies. Finally, we will discuss future directions that might be promising to unveil new insights on the coding of prehension movements.