Neuronal chains for actions in the parietal lobe: a computational model

The inferior part of the parietal lobe (IPL) is known to play a very important role in sensorimotor integration. Neurons in this region code goal-related motor acts performed with the mouth, with the hand and with the arm. It has been demonstrated that most IPL motor neurons coding a specific motor act (e.g., grasping) show markedly different activation patterns according to the final goal of the action sequence in which the act is embedded (grasping for eating or grasping for placing). Some of these neurons (parietal mirror neurons) show a similar selectivity also during the observation of the same action sequences when executed by others. Thus, it appears that the neuronal response occurring during the execution and the observation of a specific grasping act codes not only the executed motor act, but also the agent's final goal (intention).In this work we present a biologically inspired neural network architecture that models mechanisms of motor sequences execution and recognition. In this network, pools composed of motor and mirror neurons that encode motor acts of a sequence are arranged in form of action goal-specific neuronal chains. The execution and the recognition of actions is achieved through the propagation of activity bursts along specific chains modulated by visual and somatosensory inputs.The implemented spiking neuron network is able to reproduce the results found in neurophysiological recordings of parietal neurons during task performance and provides a biologically plausible implementation of the action selection and recognition process.Finally, the present paper proposes a mechanism for the formation of new neural chains by linking together in a sequential manner neurons that represent subsequent motor acts, thus producing goal-directed sequences.     

Human parietal cortex in action

Experiments using functional neuroimaging and transcranial magnetic stimulation in humans have revealed regions of the parietal lobes that are specialized for particular visuomotor actions, such as reaching, grasping and eye movements. In addition, the human parietal cortex is recruited by processing and perception of action-related information, even when no overt action occurs. Such information can include object shape and orientation, knowledge about how tools are employed and the understanding of actions made by other individuals. We review the known subregions of the human posterior parietal cortex and the principles behind their organization.     

Interpersonal Liking Modulates Motor-Related Neural Regions

Observing someone perform an action engages brain regions involved in motor planning, such as the inferior frontal, premotor, and inferior parietal cortices. Recent research suggests that during action observation, activity in these neural regions can be modulated by membership in an ethnic group defined by physical differences. In this study we expanded upon previous research by matching physical similarity of two different social groups and investigating whether likability of an outgroup member modulates activity in neural regions involved in action observation. Seventeen Jewish subjects were familiarized with biographies of eight individuals, half of the individuals belonged to Neo-Nazi groups (dislikable) and half of which did not (likable). All subjects and actors in the stimuli were Caucasian and physically similar. The subjects then viewed videos of actors portraying the characters performing simple motor actions (e.g. grasping a water bottle and raising it to the lips), while undergoing fMRI. Using multivariate pattern analysis (MVPA), we found that a classifier trained on brain activation patterns successfully discriminated between the likable and dislikable action observation conditions within the right ventral premotor cortex. These data indicate that the spatial pattern of activity in action observation related neural regions is modulated by likability even when watching a simple action such as reaching for a cup. These findings lend further support for the notion that social factors such as interpersonal liking modulate perceptual processing in motor-related cortices.     

Similar Cerebral Motor Plans for Real and Virtual Actions

A simple movement, such as pressing a button, can acquire different meanings by producing different consequences, such as starting an elevator or switching a TV channel. We evaluated whether the brain activity preceding a simple action is modulated by the expected consequences of the action itself. To further this aim, the motor-related cortical potentials were compared during two key-press actions that were identical from the kinematics point of view but different in both meaning and consequences. In one case (virtual grasp), the key-press started a video clip showing a hand moving toward a cup and grasping it; in the other case, the key-press did not produce any consequence (key-press). A third condition (real grasp) was also compared, in which subjects actually grasped the cup, producing the same action presented in the video clip. Data were collected from fifteen subjects. The results showed that motor preparation for virtual grasp (starting 3 s before the movement onset) was different from that of the key-press and similar to the real grasp preparation–as if subjects had to grasp the cup in person. In particular, both virtual and real grasp presented a posterior parietal negativity preceding activity in motor and pre-motor areas. In summary, this finding supports the hypothesis that motor preparation is affected by the meaning of the action, even when the action is only virtual.     

Sensory-motor coordination during grasping and manipulative actions.

Goal-directed grasping and manipulation of objects are human skills that depend on automatic sensory control in which predictive feed-forward mechanisms integrate somatosensory and visual signals with sensory-motor memory systems. Memory representations of physical and task-relevant properties of the object play a pivotal role. Anticipatory strategies are crucial when purposeful actions arise from learned relationships between afferent patterns and efferent commands. The development of even elementary precision grip skills is a protracted process not concluded until early adolescence. Not surprisingly, the neural control of manual actions engages most central nervous system areas known to be involved in motor control.     

Dependence of the anticipatory change in the grip force in the catching task on the result of the preceding trial

A sitting subject held a cup between the thumb and the index finger. Light or heavy objects fell into the cup in a random order. The anticipatory grip force at the moment when the falling object touched the bottom of the cup was measured. The grip force in the trials following the fall of a light object was smaller than in the trials following the fall of a heavy object and did not depend on the object mass in the current trial. Thus, the anticipatory increase in the grip force was planned on the basis of the result of the preceding trial.     

Intention Understanding in Autism

When we observe a motor act (e.g. grasping a cup) done by another individual, we extract, according to how the motor act is performed and its context, two types of information: the goal (grasping) and the intention underlying it (e.g. grasping for drinking). Here we examined whether children with autistic spectrum disorder (ASD) are able to understand these two aspects of motor acts. Two experiments were carried out. In the first, one group of high-functioning children with ASD and one of typically developing (TD) children were presented with pictures showing hand-object interactions and asked what the individual was doing and why. In half of the “why” trials the observed grip was congruent with the function of the object (“why-use” trials), in the other half it corresponded to the grip typically used to move that object (“why-place” trials). The results showed that children with ASD have no difficulties in reporting the goals of individual motor acts. In contrast they made several errors in the why task with all errors occurring in the “why-place” trials. In the second experiment the same two groups of children saw pictures showing a hand-grip congruent with the object use, but within a context suggesting either the use of the object or its placement into a container. Here children with ASD performed as TD children, correctly indicating the agent''s intention. In conclusion, our data show that understanding others'' intentions can occur in two ways: by relying on motor information derived from the hand-object interaction, and by using functional information derived from the object''s standard use. Children with ASD have no deficit in the second type of understanding, while they have difficulties in understanding others'' intentions when they have to rely exclusively on motor cues.     

How Precisely Do Bonobos (Pan paniscus) Grasp Small Objects?

The general objective of this study was to compare the precise grasping behavior and intermanual differences in performance between three Pan paniscus and five Homo sapiens in grasping small objects. We compared the temporal pattern of two submovements of consecutive grasping cycles, the (visuomotor) reaching and the (sensorimotor) grasping. Both species were similarly successful in this task, they showed a behavioral right-hand preference and preferred specific types of grips. Bonobos required less time for reaching an object but a much longer time to grasp it than humans did. Thus, the species pursued different strategies. We assumed that this might be due to the different grip techniques. However, grip preferences did not serve a quicker intramanual performance but they pronounced differences between hands. Intermanual differences in timing were restricted to the reaching part and more strongly in bonobos than in humans. However, the right hand need not necessarily perform quicker. As in the case of humans, we assume that attentional cues were focused more on preparing a proper grip with the right hand than on a quick performance. However, strong intermanual differences in bonobos may indicate an overall stronger neuronal asymmetry in the motor organization of the finger musculature that prepare a proper grip than is true of humans.     

Grasping the Intentions of Others with One's Own Mirror Neuron System

Understanding the intentions of others while watching their actions is a fundamental building block of social behavior. The neural and functional mechanisms underlying this ability are still poorly understood. To investigate these mechanisms we used functional magnetic resonance imaging. Twenty-three subjects watched three kinds of stimuli: grasping hand actions without a context, context only (scenes containing objects), and grasping hand actions performed in two different contexts. In the latter condition the context suggested the intention associated with the grasping action (either drinking or cleaning). Actions embedded in contexts, compared with the other two conditions, yielded a significant signal increase in the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. Thus, premotor mirror neuron areas—areas active during the execution and the observation of an action—previously thought to be involved only in action recognition are actually also involved in understanding the intentions of others. To ascribe an intention is to infer a forthcoming new goal, and this is an operation that the motor system does automatically.     

Grasping the intentions of others with one's own mirror neuron system

Understanding the intentions of others while watching their actions is a fundamental building block of social behavior. The neural and functional mechanisms underlying this ability are still poorly understood. To investigate these mechanisms we used functional magnetic resonance imaging. Twenty-three subjects watched three kinds of stimuli: grasping hand actions without a context, context only (scenes containing objects), and grasping hand actions performed in two different contexts. In the latter condition the context suggested the intention associated with the grasping action (either drinking or cleaning). Actions embedded in contexts, compared with the other two conditions, yielded a significant signal increase in the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. Thus, premotor mirror neuron areas—areas active during the execution and the observation of an action—previously thought to be involved only in action recognition are actually also involved in understanding the intentions of others. To ascribe an intention is to infer a forthcoming new goal, and this is an operation that the motor system does automatically.     

Event-Related Brain Potentials for Goal-Related Power Grips

Recent research has shown that neurophysiological activation during action planning depends on the orientation to initial or final action goals for precision grips. However, the neural signature for a distinct class of grasping, power grips, is still unknown. The aim of the present study was to differentiate between cerebral activity, by means of event-related potentials (ERPs), and its temporal organization during power grips executed with an emphasis on either the initial or final parts of movement sequences. In a grasp and transportation task, visual cues emphasized either the grip (the immediate goal) or the target location (the final goal). ERPs differed between immediate and final goal-cued conditions, suggesting different means of operation dependent on goal-relatedness. Differences in mean amplitude occurred earlier for power grips than for recently reported precision grips time-locked to grasping over parieto-occipital areas. Time-locked to final object placement, differences occurred within a similar time window for power and precision grips over frontal areas. These results suggest that a parieto-frontal network of activation is of crucial importance for grasp planning and execution. Our results indicate that power grip preparation and execution for goal-related actions are controlled by similar neural mechanisms as have been observed during precision grips, but with a distinct temporal pattern.     

The modulation of corticospinal excitability during motor imagery of actions with objects

We investigated whether corticospinal excitability during motor imagery of actions (the power or the pincer grip) with objects was influenced by actually touching objects (tactile input) and by the congruency of posture with the imagined action (proprioceptive input). Corticospinal excitability was assessed by monitoring motor evoked potentials (MEPs) in the first dorsal interosseous following transcranial magnetic stimulation over the motor cortex. MEPs were recorded during imagery of the power grip of a larger-sized ball (7 cm) or the pincer grip of a smaller-sized ball (3 cm)--with or without passively holding the larger-sized ball with the holding posture or the smaller-sized ball with the pinching posture. During imagery of the power grip, MEPs amplitude was increased only while the actual posture was the same as the imagined action (the holding posture). On the other hand, during imagery of the pincer grip while touching the ball, MEPs amplitude was enhanced in both postures. To examine the pure effect of touching (tactile input), we recorded MEPs during imagery of the power and pincer grip while touching various areas of an open palm with a flat foam pad. The MEPs amplitude was not affected by the palmer touching. These findings suggest that corticospinal excitability during imagery with an object is modulated by actually touching an object through the combination of tactile and proprioceptive inputs.     

Monocular vision leads to a dissociation between grip force and grip aperture scaling during reach-to-grasp movements

It has been argued that visual perception and the visual control of action depend upon functionally distinct and anatomically separable brain systems. Electrophysiological evidence indicates that binocular vision may be particularly important for the visuomotor processing within the posterior parietal cortex, and neuropsychological and psychophysical studies confirm that binocular vision is crucial for the accurate planning and control of prehension movements. An unresolved issue concerns the consequences for visuomotor processing of removing binocular vision. By one account, monocular viewing leads to reliance upon pictorial visual cues to calibrate grasping and results in disruption to normal size-constancy mechanisms. This proposal is based on the finding that maximum grip apertures are reduced with monocular vision. By a second account, monocular viewing results in the loss of binocular visual cues and leads to strategic changes in visuomotor processing by way of altered safety margins. This proposal is based on the finding that maximum grip apertures are increased with monocular vision. We measured both grip aperture and grip force during prehension movements executed with binocular and monocular viewing. We demonstrate that each of the above accounts may be correct and can be observed within the same task. Specifically, we show that, while grip apertures increase with monocular vision, consistent with altered visuomotor safety margins, maximum grip force is nevertheless reduced, consistent with a misperception of object size. These results are related to differences in visual processing required for calibrating grip aperture and grip force during reaching.     

The magic grasp: motor expertise in deception

Background

Most of us are poor at faking actions. Kinematic studies have shown that when pretending to pick up imagined objects (pantomimed actions), we move and shape our hands quite differently from when grasping real ones. These differences between real and pantomimed actions have been linked to separate brain pathways specialized for different kinds of visuomotor guidance. Yet professional magicians regularly use pantomimed actions to deceive audiences.

Methodology and Principal Findings

In this study, we tested whether, despite their skill, magicians might still show kinematic differences between grasping actions made toward real versus imagined objects. We found that their pantomimed actions in fact closely resembled real grasps when the object was visible (but displaced) (Experiment 1), but failed to do so when the object was absent (Experiment 2).

Conclusions and Significance

We suggest that although the occipito-parietal visuomotor system in the dorsal stream is designed to guide goal-directed actions, prolonged practice may enable it to calibrate actions based on visual inputs displaced from the action.     

Grasping the past. delay can improve visuomotor performance.

"Optic ataxia" is caused by damage to the human posterior parietal cortex (PPC). It disrupts all components of a visually guided prehension movement, not only the transport of the hand toward an object's location, but also the in-flight finger movements pretailored to the metric properties of the object. Like previous cases, our patient (I.G.) was quite unable to open her handgrip appropriately when directly reaching out to pick up objects of different sizes. When first tested, she failed to do this even when she had previewed the target object 5 s earlier. Yet despite this deficit in "real" grasping, we found, counterintuitively, that I.G. showed good grip scaling when "pantomiming" a grasp for an object seen earlier but no longer present. We then found that, after practice, I.G. became able to scale her handgrip when grasping a real target object that she had previewed earlier. By interposing catch trials in which a different object was covertly substituted for the original object during the delay between preview and grasp, we found that I.G. was now using memorized visual information to calibrate her real grasping movements. These results provide new evidence that "off-line" visuomotor guidance can be provided by networks independent of the PPC.     

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.     

Mutagens in coffee and tea.

Coffee prepared in the usual way for drinking contains a substance(s) that is mutagenic to Salmonella typhimurium TA100 without mammalian microsomal enzymes. One cup of coffee (200 ml) contains mutagen(s) inducing 1.4-4.6 X 10(5) revertants under standard conditions. Instant coffee too is mutagenic to TA100 and one cup of instant coffee prepared from 1 g of coffee powder and 200 ml of water induced 5.6-5.8 X 10(4) revertants of TA100. Caffeine-free instant coffee also has similar mutagenicity. Addition of microsomal enzymes abolished the mutagenicity. Black tea, green tea and Japanese roasted tea were also mutagenic to TA100 without S9 mix and one cup of these teas prepared in the ordinary way produced 1.7-3.8 X 10(4) revertants of TA100. Black tea and green tea were also mutagenic to TA98 in the presence of S9 mix after treatment with a glycosidase from Aspergillus niger, hesperidinase. This type of mutagen in one cup of black tea induced 2.4 X 10(5) revertants of TA98.     

Manual Function in Cebus apella. Digital Mobility,Preshaping, and Endurance in Repetitive Grasping

Manual dexterity varies across species of primates in accord with hand morphology and degree of fine motor control of the digits. Platyrrhine monkeys achieve less direct opposition between thumb and index finger than that of catarrhine primates, and many of them typically whole-hand grip. However, tufted capuchins (Cebus apella), exhibit a degree of independent control of the digits and effective thumb–forefinger opposition. We report how capuchins prehended small objects, with particular attention to the form of sequential fine movements of the fingers, choice of hand, and differences between the two hands in the temporal properties of reaching and grasping. We compare these actions across tasks with differing demands for fine motor control. For tasks that required all the digits to flex in synchrony, capuchins displayed smooth, fast, and efficient reach-to-grasp movements and a higher endurance than for tasks requiring more complex digital coordination. These latter tasks induced a slightly differentiated preshaping of the hand when approaching the objects, indicating preparation for grasping in advance of contact with the object. A right-hand preponderance for complex digital coordination was evident. The monkeys coordinated their fingers rather poorly at the substrate, and they took longer to achieve control of the objects when complex coordination was required than when simultaneous flexion was sufficient. We conclude that precise finger coordination is more effortful and less well coordinated, and the coordination is less lateralized, in capuchins than in catarrhine primates.     

Cascade of neural events leading from error commission to subsequent awareness revealed using EEG source imaging

The goal of the present study was to shed light on the respective contributions of three important action monitoring brain regions (i.e. cingulate cortex, insula, and orbitofrontal cortex) during the conscious detection of response errors. To this end, fourteen healthy adults performed a speeded Go/Nogo task comprising Nogo trials of varying levels of difficulty, designed to elicit aware and unaware errors. Error awareness was indicated by participants with a second key press after the target key press. Meanwhile, electromyogram (EMG) from the response hand was recorded in addition to high-density scalp electroencephalogram (EEG). In the EMG-locked grand averages, aware errors clearly elicited an error-related negativity (ERN) reflecting error detection, and a later error positivity (Pe) reflecting conscious error awareness. However, no Pe was recorded after unaware errors or hits. These results are in line with previous studies suggesting that error awareness is associated with generation of the Pe. Source localisation results confirmed that the posterior cingulate motor area was the main generator of the ERN. However, inverse solution results also point to the involvement of the left posterior insula during the time interval of the Pe, and hence error awareness. Moreover, consecutive to this insular activity, the right orbitofrontal cortex (OFC) was activated in response to aware and unaware errors but not in response to hits, consistent with the implication of this area in the evaluation of the value of an error. These results reveal a precise sequence of activations in these three non-overlapping brain regions following error commission, enabling a progressive differentiation between aware and unaware errors as a function of time elapsed, thanks to the involvement first of interoceptive or proprioceptive processes (left insula), later leading to the detection of a breach in the prepotent response mode (right OFC).     

Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions.

Patterns of precision grasp are described in stumptail macaques (Macaca arctoides) before and after lesions of the fasciculus cuneatus (FC). Three monkeys were videotaped while reaching for and grasping small food items. From these videotapes, records were made of the style and outcome of each grasp. Kinematic measurements were also made to describe grip formation and terminal grasp. During grip formation, grip aperture was measured as the distance between the tips of the index finger and the thumb. For terminal grasp, the joint angles of the index finger were measured. The majority of grasps by normal monkeys were of the precision type, in which the item was carried between the tips of the index finger and thumb. Each normal monkey approached objects with a highly consistent grip formation; that is, the fingertips formed a small grip aperture during the approach, and the aperture varied little on repeated grasps. To grasp an item, the forefinger moved in a multiarticular pattern, in which the proximal joint flexed and the distal joint extended. As a result of this combination of movements, the forefinger pad was placed directly onto the object. Following FC transection, the monkeys were studied for 10 months, beginning 1 month after the lesion, to allow for recovery from the acute effects of surgery. The monkeys could grasp the food items, but they rarely opposed the fingertips in precision grasp. Grip formation was altered and was characterized either by excessive grip aperture or by little to no finger opening. All of the monkeys used the table surface to help grasp items. Combined multiarticular patterns of flexion and extension were never observed postoperatively; they were replaced by flexion at all joints of the fingers. These results suggest that the FCs are more important for precision grasping than for other, less refined grasp forms (e.g., power grasps; Napier, 1956). The FCs provide critical proprioceptive feedback to cerebral areas involved in the planning and/or the execution of these movements.