One’s motor performance predictably modulates the understanding of others’ actions through adaptation of premotor visuo-motor neurons

Abstract

Neurons firing both during self and other's motor behavior (mirror neurons) have been described in the brain of vertebrates including humans. The activation of somatic motor programs driven by perceived behavior has been taken as evidence for mirror neurons' contribution to cognition. The inverse relation, that is the influence of motor behavior on perception, is needed for demonstrating the long-hypothesized causal role of mirror neurons in action understanding. We provide here conclusive behavioral and neurophysiological evidence for that causal role by means of cross-modal adaptation coupled with a novel transcranial magnetic stimulation (TMS)-adaptation paradigm. Blindfolded repeated motor performance of an object-directed action (push or pull) induced in healthy participants a strong visual after-effect when categorizing others' actions, as a result of motor-to-visual adaptation of visuo-motor neurons. TMS over the ventral premotor cortex, but not over the primary motor cortex, suppressed the after-effect, thus localizing the population of adapted visuo-motor neurons in the premotor cortex. These data are exquisitely consistent in humans with the existence of premotor mirror neurons that have access to the action meaning. We also show that controlled manipulation of the firing properties of this neural population produces strong predictable changes in the way we categorize others' actions.

Long- and short-term plastic modeling of action prediction abilities in volleyball

“…Furthermore, recent studies have reported action-speciWc unimodal visual and motor (Chong, Cunnington, Williams, Kanwisher, & Mattingley, 2008;Dinstein et al, 2010;Kilner, Neal, Weiskopf, Friston, & Frith, 2009;Lingnau, Gesierich, & Caramazza, 2009) as well as cross-modal adaptation of neural activity in these fronto-parietal areas (Chong et al, 2008;Dinstein et al, 2010;Kilner et al, 2009), suggesting the same neural population may be involved in the representation of speciWc actions that are either observed or executed. Importantly, repeated execution of pulling or pushing actions may induce a bias to categorize ambiguous actions as opposite to the one that had been trained, likely through a motor-tovisual adaptation of visuo-motor neurons (Cattaneo et al, 2010). Transcranial magnetic stimulation (TMS) over the inferior frontal gyrus disrupted this visual aftereVect, suggesting that this area contains mirror-like populations of neurons that are recruited in action execution and observation and may directly inXuence the visual perception of actions (Cattaneo et al, 2010).…”

“…Importantly, repeated execution of pulling or pushing actions may induce a bias to categorize ambiguous actions as opposite to the one that had been trained, likely through a motor-tovisual adaptation of visuo-motor neurons (Cattaneo et al, 2010). Transcranial magnetic stimulation (TMS) over the inferior frontal gyrus disrupted this visual aftereVect, suggesting that this area contains mirror-like populations of neurons that are recruited in action execution and observation and may directly inXuence the visual perception of actions (Cattaneo et al, 2010). Accordingly, dysfunctional activity of the inferior frontal cortex provoked by repetitive TMS or brain lesion is associated to impairments in diVerent types of action perception tasks, including: discriminating static hands with diVerent implied actions (Candidi, Urgesi, Ionta, & Aglioti, 2008;Urgesi, Candidi, Ionta, & Aglioti, 2007); estimating the weight of objects from the observation of lifting actions (Pobric & Hamilton, 2006); recognizing the correct motor performance of transitive or intransitive gestures (Pazzaglia, Smania, Corato, & Aglioti, 2008a); matching viewed gestures to their typical sound (Pazzaglia, Pizzamiglio, Pes & Aglioti, 2008b); and ordering in the correct temporal sequence a series of snapshots depicting the diVerent phases of an action (Fazio et al, 2009).…”

Observing how others lift light or heavy objects: time-dependent encoding of grip force in the primary motor cortex

“…review see Wilson & Knoblich, 2005), suggesting that 'motor simulation' in the brain is used for facilitating overt imitation and observational learning (e.g., Iacoboni et al, 1999;Rizzolatti, Fogassi, & Gallese, 2001), for understanding others' actions (de Lange et al, 2008;Jeannerod, 2001), or to track the behavior of others in real time for generating perceptual predictions (i.e., the more recent 'emulation model' on action perception (Wilson & Knoblich, 2005;Cattaneo et al, 2011). Although detailed descriptions of these models are beyond the scope of this paper, it should be noted that the various proposals are not mutually exclusive and that 'motor simulation' very likely plays a role in each of these cognitive activities (Wilson & Knoblich, 2005).…”

Visual–Motor Interactions during Action Observation Are Shaped by Cognitive Context

“…It is well known that observing anotherʼs actions influences activity in the observerʼs own motor system (visual-to-motor priming; Kilner, Paulignan, & Blakemore, 2003;Fadiga, Fogassi, Pavesi, & Rizzolatti, 1995), so that he or she is faster to initiate movements that match (or are congruent with) a concurrently observed action than to initiate movements that are mismatched (incongruent; Craighero, Bello, Fadiga, & Rizzolatti, 2002). What is less widely appreciated is that motor plans can also modulate the perceptual processing of observed actions (Bortoletto, Mattingley, & Cunnington, 2011;Cattaneo et al, 2010;Press, Gherri, Heyes, & Eimer, 2010) and influence perceptual judgments (motor-to-visual priming;Schütz-Bosbach & Prinz, 2007).…”