Caroline Catmur

Associative sequence learning: the role of experience in the development of imitation and the mirror system

A core requirement for imitation is a capacity to solve the correspondence problem; to map observed onto executed actions, even when observation and execution yield sensory inputs in different modalities and coordinate frames. Until recently, it was assumed that the human capacity to solve the correspondence problem is innate. However, it is now becoming apparent that, as predicted by the associative sequence learning model, experience, and especially sensorimotor experience, plays a critical role in the development of imitation. We review evidence from studies of non-human animals, children and adults, focusing on research in cognitive neuroscience that uses training and naturally occurring variations in expertise to examine the role of experience in the formation of the mirror system. The relevance of this research depends on the widely held assumption that the mirror system plays a causal role in generating imitative behaviour. We also report original data supporting this assumption. These data show that theta-burst transcranial magnetic stimulation of the inferior frontal gyrus, a classical mirror system area, disrupts automatic imitation of finger movements. We discuss the implications of the evidence reviewed for the evolution, development and intentional control of imitation.

Audiotactile interactions in roughness perception

The sounds produced when we touch textured surfaces frequently provide information regarding the structure of those surfaces. It has recently been demonstrated that the perception of the texture of the hands can be modified simply by manipulating the frequency content of such touch-related sounds. We investigated whether similar auditory manipulations change people’s perception of the roughness of abrasive surfaces (experiment 1). Participants were required to make speeded, forced-choice discrimination responses regarding the roughness of a series of abrasive samples which they touched briefly. Analysis of discrimination errors verified that tactile roughness perception was modulated by the frequency content of the auditory feedback. Specifically, attenuating high frequencies led to a bias towards an increased perception of tactile smoothness. In experiment 2, we replicated the rubbing-hands manipulation of previous experimenters while participants rated either the perceived roughness or wetness of their hands. The wetness scale data replicated the results in the literature, while the roughness scale data replicated the result from experiment 1. A final experiment showed that delaying the auditory feedback from the hand-rubbing reduced the magnitude of this parchment-skin illusion. These experiments demonstrate the dramatic effect that auditory frequency manipulations can have on the perceived tactile roughness and moistness of surfaces, and are consistent with the proposal that different auditory perceptual dimensions may have varying salience for different surfaces.

Attention does not modulate neural responses to social stimuli in autism spectrum disorders

We investigated whether individuals with autism spectrum disorders (ASD) would show attentional modulation for social (face) and non-social (house) stimuli. Sixteen individuals with ASD and 16 matched control participants completed a task in which pairs of face and house stimuli were present on every trial, with one of the pairs randomly assigned to attended locations and the other to unattended locations. Both mass-univariate (SPM) and region of interest analyses suggested that responses to houses were modulated by attention in both groups, but that only the control participants demonstrated attentional modulation of face-selective regions. Thus, the participants with ASD demonstrated a lack of attentional modulation which was particularly evident for the social stimulus. Analyses of effective connectivity indicated that these results were due to a failure of attention to modulate connectivity between extrastriate areas and V1. We discuss how these results may suggest a mechanism to explain the reduced salience of social stimuli in ASD.

Tactile sensitivity in Asperger syndrome

People with autism and Asperger syndrome are anecdotally said to be hypersensitive to touch. In two experiments, we measured tactile thresholds and suprathreshold tactile sensitivity in a group of adults with Asperger syndrome. In the first experiment, tactile perceptual thresholds were measured. Two frequencies of vibrotactile stimulation were used: 30 and 200 Hz. The results demonstrated significantly lower tactile perceptual thresholds in the Asperger group at 200 Hz but not at 30 Hz, thus confirming tactile hypersensitivity but only for one class of stimulus. A second experiment investigated whether self-produced movement affected the perception of touch in a group of adults with Asperger syndrome. A suprathreshold tactile stimulus was produced either by the participant (self-produced condition) or by the experimenter (externally produced condition) and participants were asked to rate the perception of the tactile stimulation. The results demonstrated that, while both Asperger and control groups rated self-produced touch as less tickly than external touch, the Asperger group rated both types of tactile stimulus as significantly more tickly and intense than did the control group. This experiment confirms the finding of tactile hypersensitivity, but shows that the perceptual consequences of self-produced touch are attenuated in the normal way in people with Asperger syndrome. An abnormality in this process cannot therefore account for their tactile hypersensitivity.

Through the looking glass: Counter-mirror activation following incompatible sensorimotor learning

The mirror system, comprising cortical areas that allow the actions of others to be represented in the observer’s own motor system, is thought to be crucial for the development of social cognition in humans. Despite the importance of the human mirror system, little is known about its origins. We investigated the role of sensorimotor experience in the development of the mirror system. Functional magnetic resonance imaging was used to measure neural responses to observed hand and foot actions following one of two types of training. During training, participants in the Compatible (control) group made mirror responses to observed actions (hand responses were made to hand stimuli and foot responses to foot stimuli), whereas the Incompatible group made counter‐mirror responses (hand to foot and foot to hand). Comparison of these groups revealed that, after training to respond in a counter‐mirror fashion, the relative action observation properties of the mirror system were reversed; areas that showed greater responses to observation of hand actions in the Compatible group responded more strongly to observation of foot actions in the Incompatible group. These results suggest that, rather than being innate or the product of unimodal visual or motor experience, the mirror properties of the mirror system are acquired through sensorimotor learning.

Making mirrors: Premotor cortex stimulation enhances mirror and counter-mirror motor facilitation

Mirror neurons fire during both the performance of an action and the observation of the same action being performed by another. These neurons have been recorded in ventral premotor and inferior parietal cortex in the macaque, but human brain imaging studies suggest that areas responding to the observation and performance of actions are more widespread. We used paired-pulse TMS to test whether dorsal as well as ventral premotor cortex is involved in producing mirror motor facilitation effects. Stimulation of premotor cortex enhanced mirror motor facilitation and also enhanced the effects of counter-mirror training. No differences were found between the two premotor areas. These results support an associative account of mirror neuron properties, whereby multiple regions that process both sensory and motor information have the potential to contribute to mirror effects.

Time course analyses confirm independence of imitative and spatial compatibility.

Imitative compatibility, or automatic imitation, has been used as a measure of imitative performance and as a behavioral index of the functioning of the human mirror system (e.g., Brass, Bekkering, Wohlschlager, & Prinz, 2000; Heyes, Bird, Johnson, & Haggard, 2005; Kilner, Paulignan, & Blakemore, 2003). However, the use of imitative compatibility as a measure of imitation has been criticized on the grounds that imitative compatibility has been confounded with simple spatial compatibility (Aicken, Wilson, Williams, & Mon-Williams, 2007; Bertenthal, Longo, & Kosobud, 2006; Jansson, Wilson, Williams, & Mon-Williams, 2007). Two experiments are reported in which, in contrast with previous studies, imitative compatibility was measured on both spatially compatible and spatially incompatible trials, and imitative compatibility was shown to be present regardless of spatial compatibility. Additional features of the experiments allowed measurement of the time courses of the imitative and spatial compatibility effects both within and across trials. It was found that imitative compatibility follows a different time course from spatial compatibility, providing further evidence for their independence and supporting the use of imitative compatibility as a measure of imitation.

Experience-based priming of body parts: a study of action imitation.

Two important dimensions of action are the movement and the body part with which the movement is effected. Experiment 1 tested whether automatic imitation is sensitive to the body part dimension of action. We found that hand and foot movements were selectively primed by observation of a corresponding, task-irrelevant effector in motion. Experiment 2 used this body part priming effect to investigate the role of sensorimotor learning in the development of imitation. The results showed that incompatible training, in which observation of hand movements was paired with execution of foot movements and vice versa, led to a greater reduction in body part priming than compatible training, in which subjects experienced typical contingencies between observation and execution of hand and foot movements. These findings are consistent with the assumption that overt behavioral imitation is mediated by the mirror neuron system, which is somatotopically organized. Our results also support the hypothesis that the development of imitation and the mirror neuron system are driven by correlated sensorimotor learning.

Alexithymia, not autism, is associated with impaired interoception

It has been proposed that Autism Spectrum Disorder (ASD) is associated with difficulties perceiving the internal state of ones body (i.e., impaired interoception), causing the socio-emotional deficits which are a diagnostic feature of the condition. However, research indicates that alexithymia – characterized by difficulties in recognizing emotions from internal bodily sensations – is also linked to atypical interoception. Elevated rates of alexithymia in the autistic population have been shown to underpin several socio-emotional impairments thought to be symptomatic of ASD, raising the possibility that interoceptive difficulties in ASD are also due to co-occurring alexithymia. Following this line of inquiry, the present study examined the relative impact of alexithymia and autism on interoceptive accuracy (IA). Across two experiments, it was found that alexithymia, not autism, was associated with atypical interoception. Results indicate that interoceptive impairments should not be considered a feature of ASD, but instead due to co-occurring alexithymia.

Timecourse of mirror and counter-mirror effects measured with transcranial magnetic stimulation

The human mirror system has been the subject of much research over the past two decades, but little is known about the timecourse of mirror responses. In addition, it is unclear whether mirror and counter-mirror effects follow the same timecourse. We used single-pulse transcranial magnetic stimulation to investigate the timecourse of mirror and counter-mirror responses in the human brain. Experiment 1 demonstrated that mirror responses can be measured from around 200 ms after observed action onset. Experiment 2 demonstrated significant effects of counter-mirror sensorimotor training at all timepoints at which a mirror response was found in Experiment 1 (i.e. from 200 ms onward), indicating that mirror and counter-mirror responses follow the same timecourse. By suggesting similarly direct routes for mirror and counter-mirror responses, these results support the associative account of mirror neuron origins whereby mirror responses arise as a result of correlated sensorimotor experience during development. More generally, they contribute to theorizing regarding mirror neuron function by providing some constraints on how quickly mirror responses can influence social cognition.