Laura Maffongelli

Listening to speech recruits specific tongue motor synergies as revealed by transcranial magnetic stimulation and tissue-Doppler ultrasound imaging

The activation of listeners motor system during speech processing was first demonstrated by the enhancement of electromyographic tongue potentials as evoked by single-pulse transcranial magnetic stimulation (TMS) over tongue motor cortex. This technique is, however, technically challenging and enables only a rather coarse measurement of this motor mirroring. Here, we applied TMS to listeners’ tongue motor area in association with ultrasound tissue Doppler imaging to describe fine-grained tongue kinematic synergies evoked by passive listening to speech. Subjects listened to syllables requiring different patterns of dorso-ventral and antero-posterior movements (/ki/, /ko/, /ti/, /to/). Results show that passive listening to speech sounds evokes a pattern of motor synergies mirroring those occurring during speech production. Moreover, mirror motor synergies were more evident in those subjects showing good performances in discriminating speech in noise demonstrating a role of the speech-related mirror system in feed-forward processing the speakers ongoing motor plan.

Vision of tongue movements bias auditory speech perception

Audiovisual speech perception is likely based on the association between auditory and visual information into stable audiovisual maps. Conflicting audiovisual inputs generate perceptual illusions such as the McGurk effect. Audiovisual mismatch effects could be either driven by the detection of violations in the standard audiovisual statistics or via the sensorimotor reconstruction of the distal articulatory event that generated the audiovisual ambiguity. In order to disambiguate between the two hypotheses we exploit the fact that the tongue is hidden to vision. For this reason, tongue movement encoding can solely be learned via speech production but not via others׳ speech perception alone. Here we asked participants to identify speech sounds while matching or mismatching visual representations of tongue movements which were shown. Vision of congruent tongue movements facilitated auditory speech identification with respect to incongruent trials. This result suggests that direct visual experience of an articulator movement is not necessary for the generation of audiovisual mismatch effects. Furthermore, we suggest that audiovisual integration in speech may benefit from speech production learning.

Representing tools as hand movements: Early and somatotopic visuomotor transformations

The term affordance defines a property of objects, which relates to the possible interactions that an agent can carry out on that object. In monkeys, canonical neurons encode both the visual and the motor properties of objects with high specificity. However, it is not clear if in humans exists a similarly fine-grained description of these visuomotor transformations. In particular, it has not yet been proven that the processing of visual features related to specific affordances induces both specific and early visuomotor transformations, given that complete specificity has been reported to emerge quite late (300-450ms). In this study, we applied an adaptation-stimulation paradigm to investigate early cortico-spinal facilitation and hand movements׳ synergies evoked by the observation of tools. We adapted, through passive observation of finger movements, neuronal populations coding either for precision or power grip actions. We then presented the picture of one tool affording one of the two grasps types and applied single-pulse Transcranial Magnetic Stimulation (TMS) to the hand primary motor cortex, 150ms after image onset. Cortico-spinal excitability of the Abductor Digiti Minimi and Abductor Pollicis Brevis showed a detailed pattern of modulations, matching tools׳ affordances. Similarly, TMS-induced hand movements showed a pattern of grip-specific whole hand synergies. These results offer a direct proof of the emergence of an early visuomotor transformation when tools are observed, that maintains the same amount of synergistic motor details as the actions we can perform on them.

Distinct brain signatures of content and structure violation during action observation

Sentences, musical phrases and goal-directed actions are composed of elements that are linked by specific rules to form meaningful outcomes. In goal-directed actions including a non-canonical element or scrambling the order of the elements alters the actions content and structure, respectively. In the present study we investigated event-related potentials of the electroencephalographic (EEG) activity recorded during observation of both alterations of the action content (obtained by violating the semantic components of an action, e.g. making coffee with cola) and alterations of the action structure (obtained by inverting the order of two temporally adjacent pictures of sequences depicting daily life actions) interfering with the normal flow of the motor acts that compose an action. Action content alterations elicited a bilateral posterior distributed EEG negativity, peaking at around 400 ms after stimulus onset similar to the ERPs evoked by semantic violations in language studies. Alteration of the action structure elicited an early left anterior negativity followed by a late left anterior positivity, which closely resembles the ERP pattern found in language syntax violation studies. Our results suggest a functional dissociation between the processing of action content and structure, reminiscent of a similar dissociation found in the language or music domains. Importantly, this study provides further support to the hypothesis that some basic mechanisms, such as the rule-based structuring of sequential events, are shared between different cognitive domains.

Beta rhythm modulation by speech sounds: somatotopic mapping in somatosensory cortex

During speech listening motor regions are somatotopically activated, resembling the activity that subtends actual speech production, suggesting that motor commands can be retrieved from sensory inputs. Crucially, the efficient motor control of the articulators relies on the accurate anticipation of the somatosensory reafference. Nevertheless, evidence about somatosensory activities elicited by auditory speech processing is sparse. The present work looked for specific interactions between auditory speech presentation and somatosensory cortical information processing. We used an auditory speech identification task with sounds having different place of articulation (bilabials and dentals). We tested whether coupling the auditory task with a peripheral electrical stimulation of the lips would affect the pattern of sensorimotor electroencephalographic rhythms. Peripheral electrical stimulation elicits a series of spectral perturbations of which the beta rebound reflects the return-to-baseline stage of somatosensory processing. We show a left-lateralized and selective reduction in the beta rebound following lip somatosensory stimulation when listening to speech sounds produced with the lips (i.e. bilabials). Thus, the somatosensory processing could not return to baseline due to the recruitment of the same neural resources by speech stimuli. Our results are a clear demonstration that heard speech sounds are somatotopically mapped onto somatosensory cortices, according to place of articulation.

Motor control may support mirror neuron research with new hypotheses and methods: reply to comments on "Grasping synergies: a motor-control approach to the mirror neuron mechanism".

We are grateful to all commentators for their insightful commentaries and observations that enrich our proposal. One of our aims was indeed to bridge the gap between fields of research that, progressing independently, are facing similar issues regarding the neural representation of motor knowledge. In this respect, we were pleased to receive feedback from eminent researchers on both the mirror neuron as well as the motor control fields. Their expertise covers animal and human neurophysiology, as well as the computational modeling of neural and behavioral processes. Given their heterogeneous cultural perspectives and research approaches, a number of important open questions were raised. For simplicity we separated these issues into four sections. In the first section we present methodological aspects regarding how synergies can be measured in paradigms investigating the human mirror system. The second section regards the fundamental definition of what exactly synergies might be. The third concerns how synergies can generate testable predictions in mirror neuron research. Finally, the fourth section deals with the ultimate question regarding the function of the mirror neuron system. Before discussing the important observations risen by commentators (Enticott [1], Frey and Chen [2], Naish and Holmes [3], Casile [4], Pezzulo, Donnarumma, Iodice, Prevete and Dindo [5], Santello [6], Swinnen and Alaerts [7], Cattaneo [8], Candidi, Sacheli and Aglioti [9], Cavallo, Ansuini and Becchio [10], de C. Hamilton [11]) we wish to stress the almost unanimous awareness that we indeed have a problem. Human mirror neuron research has almost ended up in a theoretical cul de sac, and we are in need for new falsifiable models on the function of this system [12]. We are very pleased to observe that our aim to infuse some fresh blood, coming from more mature fields of research, was appreciated by almost all commentators, giving raise to intriguing new suggestions.

Syntactical regularities of action sequences in the infant brain: when structure matters

Throughout life, actions and language are inherent to social interactions. A long-standing research question in cognitive neuroscience concerns the interrelation between verbal and non-verbal forms of social interactions, that is, language and action. Perceiving how actions are performed and why they are performed in a certain way is crucial for the observer to anticipate the actors goal and to prepare an appropriate response. It is suggested that predicting upcoming events in a given action sequence can be compared to the way we process the language information flow. Goal-directed actions can be sequenced in small units, which are organized according to a hierarchical plan, resembling the hierarchical organization of language. Research on adults suggests that manipulating the action structure (i.e., action syntax) leads to analogous cortical signatures as a similar manipulation of a sentence structure (i.e., language syntax). Whereas in adults language and action knowledge are based on life-time experience, in infants both domains are still developing. The current study examined the neural processing of structural violations of observed goal-directed action sequences in infants at 6-7 months, using event-related potentials (ERPs). Results showed that a structural violation of the action sequence elicited bilateral frontal positivity effects. This suggests that infants capture structural regularities, and it adds a crucial element to the understanding of general syntactic regularities and their violation from an ontogenetic perspective.