The Role of the Dorsal Premotor and Superior Parietal Cortices in Decoupled Visuomotor Transformations

In order to successfully interact with objects located within our environment, the brain must be capable of combining visual information with the appropriate felt limb position (i.e. proprioception) in order compute an appropriate coordinated muscle plan for accurate motor control. Eye-hand coordination is essential to our independence as a species and relies heavily on the reciprocally-connected regions of the parieto-frontal reach network. The dorsal premotor cortex (PMd) and the superior parietal lobule (SPL) remain prime candidates within this network for controlling the transformations required during visually-guided reaching movements. Our brains are primed to reach directly towards a viewed object, a situation that has been termed a “standard” or coupled reach. Such direct eye-hand coordination is common across species and is crucial for basic survival. Humans, however, have developed the capacity for tool-use and thus have learned to interact indirectly with an object. In such “non-standard” or decoupled situations, the directions of gaze and arm movement have been spatially decoupled and rely on both the implementation of a cognitive rule and on online feedback of the decoupled limb. The studies included within this dissertation were designed to further characterize the role of PMd and SPL during situations in which when a reach requires a spatial transformation between the actions of the eyes and the hand. More specifically, we were interested in examining whether regions within PMd (PMdr, PMdc) and SPL (PEc, MIP) responded differently during coupled versus decoupled visuomotor transformations. To address the relative contribution of these various cortical regions during decoupled reaching movements, we trained two female rhesus macaques on both coupled and decoupled visually-guided reaching tasks. We recorded the neural activity (single units and local field potentials) within each region while the animals performed each condition. We found that two separate networks emerged each contributing in a distinct ways to the performance of coupled versus decoupled eye-hand reaches. While PMdr and PEc showed enhanced activity during decoupled reach conditions, PMdc and MIP were more enhanced during coupled reaches. Taken together, these data presented here provide further evidence for the existence of alternate task-dependent neural pathways for visuomotor integration

Specific Roles Of Macaque Parietal Regions In Making Saccades And Reaches

A principle task of our brain is to guide movements, includng saccade: fast eye movements) and reaches towards things that we see. Regions in the parietal cortex such as LIP and PRR are active during visually-guided movements. Neurons in these areas respond differentially for saccades versus reaches, but in most parietal areas there is some response: in single unit recording as well as in fMRI imaging) with either type of movement. This raises an important question. What is the functional significance of the neuronal activity in parietal areas? Recording and imaging studies can only show correlations; causal roles must be inferred. The activity in any particular area could reflect where the subject\u27s spatial attention is directed, without regard for what behavior the subject will perform. Stronger activity in one task compared to another could reflect differential allocation of attention. For example, we might attend more strongly to a target for an eye movement than to a target for an arm movement, or vice versa. Alternatively, might play a causal role in driving only one type of movement. In this case, the weaker activity evoked during a different type of movement might serve no purpose at all; it might represent a contingency plan to perform the non-selected movement; or it might be serve some other function unrelated to the specific movement - for example, weak saccade-related activity in an area with strong arm movement related signals might support play no role in driving eye movements, but instead provide timing information to the reaching system to support eye-hand coordination. To help resolve this mystery, we used an interventional approach. We asked what happens to reaches and saccades when we reversibly lesioned specific areas in the monkey parietal cortex. In order to establish what brain regions were affected in each inactivation experiment, we developed a novel technique to image the location of the lesions in vivo. The results of this causal manipulation were clear: LIP lesions delay the initiation of saccades and have no effect on reaches, while PRR lesions delay the initiation of reaches and have no effect on saccades. We obtained further evidence for a more motoric role for parietal areas than previously suspected. PRR was active for reaches of only the contralateral arm, aimed at targets in either hemisphere - similar to the typical profiles of motor but not visual sensory areas. Interestingly, LIP lesions did influence reaches, but only when the animals were allowed to first look at the target before reaching for it. We believe that in this case, the reaching movement waits for the saccade system, and so the direct effect of the lesion on the saccades has an indirect effect on the reaches. These results are important for several reasons. First, they resolve a long-standing debate regarding the functional specificity of parietal areas with regard to particular movements and attention. They provide new information on the circuits guiding eye movements, arm movements and eye-hand coordination. Finally, our results underscore the fact that measurements of neuronal activity can be misleading, and are only one of several tools that must be used in order to understand brain function

Neural basis of motor planning for object-oriented actions: the role of kinematics and cognitive aspects

The project I have carried out in these three years as PhD student pursued the aim of describing the motor preparation activity related to the object oriented actions actually performed. The importance of these studies comes from the lack of literature on EEG and complex movements actually executed and not just mimed or pantomimed. Using the term ‘complex’ here we refer to actions that are oriented to an object with the intent to interact with it. In order to provide a broader idea about the aim of the project, I have illustrated the complexity of the movements and cortical networks involved in their processing and execution. Several cortical areas concur to the plan and execution of a movement, and the contribution of these different areas changes according to the complexity, in terms of kinematics, of the action. The object-oriented action seems to be a circuit apart: besides motor structures, it also involves a temporo-parietal network that takes part to both planning and performing actions like reaching and grasping. Such findings have been pointed out starting from studies on the Mirror neuron system discovered in monkeys at the beginning of the ‘90s and subsequently extended to humans. Apart from all the speculations this discovery has opened to, many different researchers have started investigating different aspects related to reaching and grasping movements, describing different areas involved, all belonging to the posterior parietal cortex (PPC), and their connections with anterior motor cortices through different paradigms and techniques. Most of the studies investigating movement execution and preparation are studies on monkey or fMRI studies on humans. Limits of this technique come from its low temporal resolution and the impossibility to use self-paced movement, that is, movement performed in more ecological conditions when the subject decides freely to move. On the few studies investigating motor preparation using EEG, only pantomime of action has been used, more than real interactions with objects. Because all of these factors, we decided to get through the description of the motor preparation activity for goal oriented actions pursuing two aims: in the first instance, to describe this activity for grasping and reaching actions actually performed toward a cup (a very ecological object); secondly, we wanted to verify which parameters in these kind of movements are taken into account during their planning and preparation: because of all the variables involved in grasping and reaching movements, like the position of the objects, its features, the goal of the action and its meaning, we tried to verify how these variables could affect motor preparation creating two different experiments. In the first one, subjects were requested to perform a grasping and a reaching action toward a cup and in a third condition we tied up their hands as fist in order to verify what it could happen when people are in the condition of turning an ordinary and easy action into a new one to accomplish the final task requested. In the second experiment, we better accounted for the cognitive aspects beyond the motor preparation of an action. Here, indeed, we tested a very simple action like a key press in two different conditions. In the first one the button press was not related to any kind of consequence, whereas in the second case the same action triggered a video on a screen showing a hand moving toward a cup and grasping it (giving like a video-game effect). Both the experiments have shown results straightening the role cognitive processes have in motor planning. In particular, it seemed that the goal of the action, along with the object we are going to interact with, could create a particular response and activity starting very early in the posterior parietal cortex. Finally, because of the actions used in these experiments, it was important testing the hypothesis that our findings could be generalized even to the observation of those same actions. As I mentioned before, object-oriented actions have received great attention starting from the discovery of the mirror neuron system which showed a correspondence between the cortical activity of the person performing the action with the one produced in the observer. Such a finding allowed to describe our brain as a social brain, able to create a mental representation of what the other person is doing which allows us to understand others gesture and intentions. What we wanted to test in this project was the possibility that such a correspondence between the observer and the actor would had been extended even to the motor preparation period of an upcoming action, giving credit to the hypothesis of considering the human brain as able to even predict others actions and intentions besides understanding them. In the last experiment I carried out in my project, thus, I used the same actions involved in the first experiment but asking this time to observe them passively instead of performing them. The results provided in this study confirmed the cognitive, rather than motor, role the PPC plays in action planning. Indeed, even when no movements are involved, the same structure are active reflecting the activity found in the execution experiment. The main result I have reported in this dissertation is related to the suggestion of a new model to understand the role the PPC has in object-oriented movements. Unlike previous hypothesis and models suggesting the contribution of PPC in extracting affordances from the objects or monitoring and transforming coordinates between us and the object into intention for acting, we suggest here that the role of the parietal areas is more to make a judge about the appropriate match of the action goal with the affordances provided by the object. When actually the action we are going to perform fits well with the object features, the PPC starts its activity, elaborating all those coordinates representation and monitoring the execution and programming phases of movement. This model is well supported by results from both our experiments and well combines the two previous models, but putting more emphasis on the ‘goal-object matching’ function of the PPC and the Superior parietal lobe (SPL) in particular

Neural representation of movement tau

A fundamental aspect of goal‐directed behaviour concerns the closure of motion‐gaps in a timely fashion. An influential theory about how this can be achieved is provided by the tautheory (Lee, 1998). Tau is defined as the ratio of the current distance‐to‐goal gap over the current instantaneous speed towards the goal. In this work we investigated the neural representation of tau in two sets of experiments. In one study we recorded neuromagnetic fluxes (using magnetoencephalography, MEG) from the whole brain of human subjects performing discrete hand movements aimed to targets in space, whereas the other study involved recordings of single cell activity from prefrontal and posterior parietal areas of a behaving monkey during geometrical shape‐copying tasks. These two studies provided complementary information, for the former covered the whole brain (at the cost of weak localization), whereas the latter used the finest neural grain (at the expense of limited brain regions). However, the two studies together yielded valuable information concerning the dynamic, time‐varying neural representation of tau, with respect to both integrated synaptic events in neuronal ensembles (recorded by MEG) and neural spike outputs (recorded by microelectrodes). The relations between neural signals and tau were analyzed using a linear regression model where the time‐varying neural signal (magnetic field strength in fT or spike density function) was the dependent variable and the corresponding value of movement tau and speed were the independent variables. In addition, the model included an autoregressive term to account for the expected correlated errors, given the time series nature of the data. The neurophysiological study revealed a statistically significant (p < 0.05) relation of spike density function to tau (in the presence or absence of a significant speed effect) in 17% of cells in the posterior parietal cortex (N = 399) and 8% of cells in the prefrontal cortex (N = 163). These results are in accord with previous findings in an interception task. The MEG study revealed that a mean of 21.98 (± 6.08) % of sensor signals had a statistically significant (p < 0.05) relation to tau across all subjects. These effects were distributed predominantly over the left parietal‐temporo‐occipital sensor space, with additional foci over the frontal sensorimotor regions. Altogether, these findings demonstrate a specific involvement of neurons and neuronal ensembles with the tau variable and pave the way for further studies on predictive tau control