Decoding grip type and action goal during the observation of reaching-grasping actions: A multivariate fMRI study

During execution and observation of reaching-grasping actions, the brain must encode, at the same time, the final action goal and the type of grip necessary to achieve it. Recently, it has been proposed that the Mirror Neuron System (MNS) is involved not only in coding the final goal of the observed action, but also the type of grip used to grasp the object. However, the specific contribution of the different areas of the MNS, at both cortical and subcortical level, in disentangling action goal and grip type is still unclear. Here, twenty human volunteers participated in an fMRI study in which they performed two tasks: (a) observation of four different types of actions, consisting in reaching-to-grasp a box handle with two possible grips (precision, hook) and two possible goals (open, close); (b) action execution, in which participants performed grasping actions similar to those presented during the observation task. A conjunction analysis revealed the presence of shared activated voxels for both action observation and execution within several cortical areas including dorsal and ventral premotor cortex, inferior and superior parietal cortex, intraparietal sulcus, primary somatosensory cortex, and cerebellar lobules VI and VIII. ROI analyses showed a main effect for grip type in several premotor and parietal areas and cerebellar lobule VI, with higher BOLD activation during observation of precision vs hook actions. A grip x goal interaction was also present in the left inferior parietal cortex, with higher BOLD activity during precision-to-close actions. A multivariate pattern analysis (MVPA) revealed a significant accuracy for the grip model in all ROIs, while for the action goal model, significant accuracy was observed only for left inferior parietal cortex ROI. These findings indicate that a large network involving cortical and cerebellar areas is involved in the processing of type of grip, while final action goal appears to be mainly processed within the inferior parietal region, suggesting a differential contribution of the areas activated in this study

Funzioni di alto livello nella corteccia somatosensoriale secondaria (SII)

Le proprietà della corteccia somato-sensoriale secondaria (SII) sono state largamente discusse in molteplici studi sia nella scimmia, sia nell’uomo, suggerendo che quest’area assolva funzioni di alto livello nel processamento dello stimolo tattile, quali, ad esempio, l’apprendimento o la memoria. Recentemente, alcuni studi su scimmia hanno evidenziato che, oltre agli stimoli somato-sensoriali, SII risponde anche alla stimolazione dello spazio peri-personale, all’esecuzione di azioni, alla vista di oggetti in movimento ed all’osservazione di azioni, candidando SII ad essere un’area complessa, non limitata a sole funzioni somato-sensoriali. Partendo dallo studio delle risposte di SII agli stimoli tattili, lo scopo di questa tesi è di investigare la risposta di quest’area a stimoli complessi, con particolare attenzione a task di integrazione visuo-tattile e all’osservazione di azioni nell’uomo. Con queste finalità, gli esperimenti presentati sono stati condotti mediante elettroencefalografia stereotassica (stereo-EEG) su pazienti epilettici farmaco-resistenti, impiantati come parte della loro valutazione pre-chirurgica. In una prima fase, sono stati studiati la distribuzione spaziale ed il profilo temporale delle risposte intra-corticali alla stimolazione del nervo mediano controlaterale ed ipsilaterale. I risultati ottenuti indicano che mentre la corteccia somato-sensoriale primaria (SI), il giro precentrale ed il solco intra-parietale rispondono solo alla stimolazione controlaterale, la corteccia somato-sensoriale secondaria e l’insula posteriore sono attivate bilateralmente. Inoltre, queste ultime sono caratterizzate da una risposta tonica e duratura nel tempo. Questa potrebbe rappresentare un meccanismo di ritenzione temporale dell’informazione tattile ed essere l’espressione di funzioni di alto livello quali appunto la memoria e l’apprendimento degli stimoli. Nella seconda sezione della tesi, per testare il possibile coinvolgimento dell’opercolo parietale nell’integrazione visuo-tattile, la stimolazione del nervo mediano controlaterale è stata somministrata congiuntamente ad una stimolazione visiva (i.e. flash). I risultati ottenuti evidenziano un aumento in ampiezza della componente tonica, se comparato alla sola stimolazione tattile, localizzato nell’insula posteriore e nelle porzioni più rostrali dell’opercolo parietale mentre SII mostra un comportamento del tutto inalterato. Tuttavia, tenendo in considerazione che studi su primati non umani riportano risposte visiva in SII a stimoli biologici, sono necessarie ulteriori indagini per comprendere quale tipologia di stimolazione determina l’attivazione di quest’area. Infine, la terza parte della tesi mostra le risposte intra-corticali di SI e SII ad un task motorio che include compiti di afferramento e manipolazione di oggetti, e all’osservazione delle stesse azioni eseguite da un altro individuo. I risultati evidenziano un’attivazione bilaterale di SII, sia durante l’esecuzione sia durante l’osservazione di azioni, con un profilo temporale sincrono. Al contrario SI è attiva solo durante l’esecuzione: l’input a SI durante l’osservazione non ha dunque una natura somato-sensoriale ma piuttosto deve essere sostenuto da un circuito visuo-motorio capace di operare in maniera simultanea. In conclusione, questa tesi dimostra il ruolo cruciale di SII non solo nel processamento degli stimoli tattili ma anche nell’integrazione di stimoli visuo-motori.The somatosensory properties of the second somatosensory cortex (SII) have been largely described by many studies in both monkeys and humans, suggesting for this area a high-order role in tactile stimulation processing with functions including tactile learning and memory. More interestingly, recent studies on monkeys showed that beyond somatosensory stimuli, SII responds to a wider number of stimuli including peripersonal space stimulation, active movements, observation of objects displacement and action observation. Taking into account these results, SII is a candidate to be more than just a somatosensory area. Starting from its somatosensory properties, this thesis aims to disentangle the role of SII in more complex tasks with particular attention to visuo-tactile integration and action observation in humans. To this purpose, the experiments presented in this thesis are carried with stereotactic electroencephalography (stereo-EEG) on drug-resistant epileptic patients to take advantage of its high temporal and spatial resolution. Firstly, I investigated the spatial distribution and the temporal profile of the intracortical responses to both contralateral and ipsilateral median nerve stimulation. Results indicated that while the primary somatosensory area, precentral gyrus and intra-parietal sulcus respond only to the contralateral stimulation, the secondary somatosensory cortex and posterior insula are activated bilaterally. Furthermore, these regions exhibit a tonic long-lasting temporal profile, which might represent a mechanism of temporal retention of the tactile information, and thus be the signature of high-level somatosensory functions such as tactile memory and awareness. In a second stage of the thesis, to test the possible involvement of parietal operculum in visuo-tactile integration, we administered to patients contralateral median nerve stimulation jointly with visual stimulation (i.e. flash) to about 100 drug-resistant epileptic patients. Results underline an enhancement of the tonic components relative to tactile stimulation only, limited to posterior insula and to the rostral areas of parietal operculum, with SII maintaining an unaltered behavior. Considering previous findings in non-human primates, which reported visual responses in SII in response to biological stimuli, further researches are needed to understand which threshold in the stimulus might determine the eventual activation of this area. With this aim, the third part of this thesis presents the intracortical responses of both SI and SII to a motor task requiring reaching, grasping and manipulation, as well as to the observation of the same actions performed by another individual. The results obtained highlighted that SII activates bilaterally, both during the execution and the observation of actions, with a synchronous temporal profile. Conversely, SI activates only during the execution, leading to the conclusion that the input to SII during the observation condition has not a somatosensory nature, but rather that it is sustained by visuo-motor circuits operating simultaneously. Taking together all the evidence, this thesis demonstrates the pivotal role of SII not only in somatosensory functions, as largely reported in literature, but also in the integration of visuo-motor stimuli

Anterior Intraparietal Area: a Hub in the Observed Manipulative Action Network.

Current knowledge regarding the processing of observed manipulative actions (OMAs) (e.g., grasping, dragging, or dropping) is limited to grasping and underlying neural circuitry remains controversial. Here, we addressed these issues by combining chronic neuronal recordings along the anteroposterior extent of monkeys\u2019 anterior intraparietal (AIP) area with tracer injections into the recorded sites. We found robust neural selectivity for 7 distinct OMAs, particularly in the posterior part of AIP (pAIP), where it was associated with motor coding of grip type and own-hand visual feedback. This cluster of functional properties appears to be specifically grounded in stronger direct connections of pAIP with the temporal regions of the ventral visual stream and the prefrontal cortex, as connections with skeletomotor related areas and regions of the dorsal visual stream exhibited opposite or no rostrocaudal gradients. Temporal and prefrontal areas may provide visual and contextual information relevant for manipulative action processing. These results revise existing models of the action observation network, suggesting that pAIP constitutes a parietal hub for routing information about OMA identity to the other nodes of the network

The cognitive neuroscience of visual working memory

Visual working memory allows us to temporarily maintain and manipulate visual information in order to solve a task. The study of the brain mechanisms underlying this function began more than half a century ago, with Scoville and Milner’s (1957) seminal discoveries with amnesic patients. This timely collection of papers brings together diverse perspectives on the cognitive neuroscience of visual working memory from multiple fields that have traditionally been fairly disjointed: human neuroimaging, electrophysiological, behavioural and animal lesion studies, investigating both the developing and the adult brain

How the brain grasps tools: fMRI & motion-capture investigations

Humans’ ability to learn about and use tools is considered a defining feature of our species, with most related neuroimaging investigations involving proxy 2D picture viewing tasks. Using a novel tool grasping paradigm across three experiments, participants grasped 3D-printed tools (e.g., a knife) in ways that were considered to be typical (i.e., by the handle) or atypical (i.e., by the blade) for subsequent use. As a control, participants also performed grasps in corresponding directions on a series of 3D-printed non-tool objects, matched for properties including elongation and object size. Project 1 paired a powerful fMRI block-design with visual localiser Region of Interest (ROI) and searchlight Multivoxel Pattern Analysis (MVPA) approaches. Most remarkably, ROI MVPA revealed that hand-selective, but not anatomically overlapping tool-selective, areas of the left Lateral Occipital Temporal Cortex and Intraparietal Sulcus represented the typicality of tool grasping. Searchlight MVPA found similar evidence within left anterior temporal cortex as well as right parietal and temporal areas. Project 2 measured hand kinematics using motion-capture during a highly similar procedure, finding hallmark grip scaling effects despite the unnatural task demands. Further, slower movements were observed when grasping tools, relative to non-tools, with grip scaling also being poorer for atypical tool, compared to non-tool, grasping. Project 3 used a slow-event related fMRI design to investigate whether representations of typicality were detectable during motor planning, but MVPA was largely unsuccessful, presumably due to a lack of statistical power. Taken together, the representations of typicality identified within areas of the ventral and dorsal, but not ventro-dorsal, pathways have implications for specific predictions made by leading theories about the neural regions supporting human tool-use, including dual visual stream theory and the two-action systems model

Investigation of the multiple-demand network at multiple spatial scales

This dissertation investigates the frontoparietal ‘multiple-demand’ (MD) network that is involved in the processing of diverse cognitive demands. This network is active when the task at hand is made more demanding, in a variety of different tasks including working memory, task switching, inhibition, math, language etc. While the different MD regions have partly different functions, they are highly interconnected allowing them to function together as a network. The experiment in Chapter 2 looked at the interplay between functional differences as well as co-recruitment within this multiple-demand network. Quantitative differences between regions were more prominent in simple tasks. A strong co-recruitment was seen with increased challenge or incentive. In Chapter 3, task preferences were studied at the voxel level. MD regions were equally well localised in single-subjects using any of three task demands. Voxels localised by all three tasks also captured the underlying neural representations to a similar level in a separate criterion task. Chapter 4 investigated if task representations, as measured by multi-voxel patterns, were modified due to external motivation. The effect was limited to the cue phase and did not extend to the stimulus processing phase where the stimulus is integrated with the cue to arrive at the response. Chapter 5 examined neural representations in frontal and parietal regions more directly through single unit activity and local field potentials (LFPs), during a spatial working memory task. While single neurons showed dynamic coding of target information rather than persistent coding, LFPs held this information constant through time. The impact of reference voltages on LFP data was further investigated. Together, these results explore the functional differences between and within the MD regions, and provide evidence for flexible task representations at the voxel and neuronal level.Funded by Gates Cambridg

Understanding motor planning and action recognition of pantomimed grasps

The ability to manipulate objects with considerable skill is one of the defining features of primates. In both humans and non-human primates, grasping is typically directed toward a visible object and results in contact with the object. Humans - and perhaps some other species - are also capable of grasping imaginary objects in a pantomimed prehension. Pantomimed grasps are well studied, both for theoretical and clinical interests, to explore the double function of human hands, as instrumental as well as communicative devices. The present thesis aims to investigate both aspects of pantomimed grasps in terms of motor control, action understanding and neural activation during action observation. The first experiment explored whether the way pantomimed grasps are executed can convey weight information of imaginary objects. The second experiment tested whether observers can exploit movement kinematics to discriminate between real (i.e., movements directed toward a physically present object) and pantomimed grasps. The third study investigated if perception of real and pantomimed grasps might automatically drive object representation. The fourth experiment inspected whether having a motor expertise on pantomimed grasp execution impacts pantomimed grasp processing. The fifth experiment shed new insights on the neural underpinnings of action understanding mechanisms by exploring electroencephalography (EEG) signals during real and pantomimed grasp observation

25th Annual Computational Neuroscience Meeting: CNS-2016

Abstracts of the 25th Annual Computational Neuroscience Meeting: CNS-2016 Seogwipo City, Jeju-do, South Korea. 2–7 July 201

25th annual computational neuroscience meeting: CNS-2016

The same neuron may play different functional roles in the neural circuits to which it belongs. For example, neurons in the Tritonia pedal ganglia may participate in variable phases of the swim motor rhythms [1]. While such neuronal functional variability is likely to play a major role the delivery of the functionality of neural systems, it is difficult to study it in most nervous systems. We work on the pyloric rhythm network of the crustacean stomatogastric ganglion (STG) [2]. Typically network models of the STG treat neurons of the same functional type as a single model neuron (e.g. PD neurons), assuming the same conductance parameters for these neurons and implying their synchronous firing [3, 4]. However, simultaneous recording of PD neurons shows differences between the timings of spikes of these neurons. This may indicate functional variability of these neurons. Here we modelled separately the two PD neurons of the STG in a multi-neuron model of the pyloric network. Our neuron models comply with known correlations between conductance parameters of ionic currents. Our results reproduce the experimental finding of increasing spike time distance between spikes originating from the two model PD neurons during their synchronised burst phase. The PD neuron with the larger calcium conductance generates its spikes before the other PD neuron. Larger potassium conductance values in the follower neuron imply longer delays between spikes, see Fig. 17.Neuromodulators change the conductance parameters of neurons and maintain the ratios of these parameters [5]. Our results show that such changes may shift the individual contribution of two PD neurons to the PD-phase of the pyloric rhythm altering their functionality within this rhythm. Our work paves the way towards an accessible experimental and computational framework for the analysis of the mechanisms and impact of functional variability of neurons within the neural circuits to which they belong