Impairment of actions chains in autism and its possible role in intention understanding

Abstract

Experiments in monkeys demonstrated that many parietal and premotor neurons coding a specific motor act (e.g., grasping) show a markedly different activation when this act is part of actions that have different goals (e.g., grasping for eating vs. grasping for placing). Many of these ''action-constrained'' neurons have mirror properties firing selectively to the observation of the initial motor act of the actions to which they belong motorically. By activating a specific action chain from its very outset, this mechanism allows the observers to have an internal copy of the whole action before its execution, thus enabling them to understand directly the agent's intention. Using electromyographic recordings, we show that a similar chained organization exists in typically developing children, whereas it is impaired in children with autism. We propose that, as a consequence of this functional impairment, high-functioning autistic children may understand the intentions of others cognitively but lack the mechanism for understanding them experientially.mirror neurons ͉ motor chains ͉ motor acts ͉ goal understanding ͉ motor intention H umans and monkeys possess a neural system, called the mirror neuron system, that maps visual descriptions of actions done by others onto the observer's motor representations of the same actions (1). In humans, the mirror neuron system has two major components. One is formed by the inferior parietal lobule and the ventral premotor cortex plus the caudal part of Broca's area, the other by the insula and anterior cingulate gyrus (1, 2).The mirror neuron system does not possess a unique function. Besides its originally proposed role in action understanding, its parieto-frontal component appears to mediate the understanding of intentions of others (3) and imitation (4-7), whereas its insular-cingulate component appears to play a fundamental role in emotion recognition (2,8).Recent data obtained in the monkey revealed that the mirror neuron mechanism underlying intention understanding relies on the activation of a specific set of ''action-constrained'' parietal neurons (9). These neurons discharge in association with specific motor acts but become maximally activated when the coded motor act is embedded into a specific motor action. Thus, for example, action-constrained grasping neurons strongly discharge when grasping a piece of food is followed by bringing it to the mouth, but not when it is followed by placing it into a container. Most interestingly, many action-constrained neurons have mirror properties. These neurons selectively discharge when the observation of motor acts is part of a given action (e.g., grasping for eating but not grasping for placing) (9). Their activation provides, therefore, information on the fact that an individual is grasping, but most importantly also gives clues on why the individual is doing it. Through this mechanism the observer, besides recognizing the observed motor act, is also able to predict what will be the final goal of the action. In other words, the ob...

The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations

“…How can the discrepancy between imaging and electrophysiological findings and behavioural data be explained? An answer has been provided by a study in which children with ASD were asked to grasp a piece of food either for eating or for placing in a container (see the figure, part a) and, in another set-up, to observe an experimenter performing these actions 85 . The activity of the mylohyoid (MH) muscle, which is involved in mouth opening, was recorded to produce an electromyograph (EMG).…”

“…cattaneo and colleagues tested whether the understanding of motor intention in humans might be based on the 'chain mechanism' described in the monkey 85 . participants were asked to grasp a piece of food and eat it or to grasp a piece of food and place it in a container.…”

What can autism teach us about the role of sensorimotor systems in higher cognition? New clues from studies on language, action semantics, and abstract emotional concept processing

“…The mechanism of this perception-to-action mapping has been posited in mirror neurons, a type of sensorimotor neuron 7 responsive both when a specific action is carried out and when the same action type is perceived visually or acoustically (Rizzolatti & Sinigaglia, 2010). Neural activity attributable to mirror neurons in premotor and motor cortex is abnormally low in ASC (Bernier, Dawson, Webb, & Murias, 2007;Cattaneo et al, 2007;Dapretto et al, 2006;Honaga et al, 2010;McCleery et al, 2013;Nishitani, Avikainen, & Hari, 2004;Oberman et al, 2005;Rizzolatti & Fabbri-Destro, 2010;Theoret et al, 2005;Wadsworth et al, 2017), 8 and therefore was interpreted as support for proposals that the autistic phenotype results from the dysfunction of mirror neuron systems (the 'broken mirrors' hypothesis: Ramachandran & Oberman, 2006).…”

Understanding the mechanisms behind deficits in imitation: Do individuals with autism know ‘what’ to imitate and do they know ‘how’ to imitate?

“…Second, the research group of Rizzolatti has postulated that the primary deficit is not the responsiveness of the hMNS to the observation of others' actions, but the impaired organization of motor chains underlying the action representations (Cattaneo et al, 2007;Fabbri-Destro, Cattaneo, Boria, & Rizzolatti, 2009). They draw attention to the recent finding of action-constrained parietal mirror neurons in monkeys.…”

“…Children with autism systematically attributed to the demonstrator the intention that could be derived by the semantics of the object per se (e.g., an intention to eat when food was shown) regardless of how the object was grasped (Cattaneo et al, 2007). Although studies have yielded inconsistent findings, there is some evidence of visuomotor mapping problems involving the hMNS underlying imitation problems in autism.…”