The shared circuits model (SCM) has much in common with existing models of complex behavior and relies on some known properties of the nervous system. For example, most researchers no longer hold a pure version of the “sandwich model” and assume that perception and action overlap at the level of representation. Similarly, most agree that imitation exists on a continuum, with complex forms of true imitation relying on and evolving from more simple forms of reflexive imitation. In addition, there is general agreement that mirror neurons and forward models are relevant to questions about how we bridge the intersubjective divide and model others as we do ourselves. Therefore, most of Hurley's theoretical review is consistent with existing theory and data on the mechanisms of complex interpersonal phenomena, making it unlikely that anyone will take issue with the basic premises of the model; on the flip side, this also means that the model is limited in its ability to stimulate new directions for the field.
The five-layer model is the unique contribution of the model. However, I think that this part of the model suffers from being pitched at the functional/informational level. This is unfortunate and unnecessary given that much of the theory relies on very specific mechanisms for motor control and perspective taking that are precisely defined and empirically supported. Hence, the model could have been aimed at a functional neuroanatomical level, which would have made it more specific and more accurate.
The model also seems both underspecified and overspecified. In places where the literature is most agnostic on how certain processes work, Hurley is also agnostic. For example, the model intermixes concrete and abstract concepts (such as “targets,” which can be either motor goals or life plans) without specifying whether we use the same neural processes for both, or just use analogous processes when planning to reach for a cup or to overthrow the government. In contrast, the formulation of the model into five discrete layers seems ill-fated, limiting the ability of the model to accord with the structure and functions of the nervous system. For example, layers 1 and 2 likely overlap a great deal in the brain because both require the cerebellum and act in concert to control action (cf. Wolpert et al. Reference Wolpert, Miall and Kawato1998). Conversely, there is no reason from phylogeny or ontogeny to assume that these two layers of control are primary to or evolved before the mirroring mechanisms of layer 3. Layer 2 focuses on visual and tactile feedback from the periphery, which are actually slow forms of feedback that forward models were designed to surpass. Layer 4 focuses almost entirely on “monitored inhibition” to segregate activation related to self and other, but it is unclear which type of inhibition is inculcated here (spinal, brain stem, frontal?), and there are many other ways in which self and other activation can be differentiated. Thus, it seems that there are ambiguities and inconsistencies in the model that could have been rectified by making more specific reference to the existing data on how the brain processes information.
Our lab seeks to understand the ways in which people process and understand the emotions of others. Like Hurley, we believe that basic emotion processing and related intersubjective phenomena, such as empathy, rely on an evolutionary conserved and basic perception-action mechanism (PAM) whereby perception of the emotional state of another automatically activates one's own representations for the state and situation (Preston & de Waal Reference Preston and de Waal2002).
Supporting Hurley's general rejection of the sandwich model, functional imaging work on empathy has found overlap between self and other processes in regions associated with subjective feeling states (Jackson et al. Reference Jackson, Brunet, Meltzoff and Decety2006; Lamm et al. Reference Lamm, Batson and Decety2007; Preston et al. Reference Preston, Bechara, Damasio, Grabowski, Stansfield, Mehta and Damasio2007; in preparation b; Singer et al. Reference Singer, Seymour, O'Doherty, Kaube, Dolan and Frith2004; Reference Singer, Seymour, O'Doherty, Klaas, Dolan and Frith2006). Further supporting Hurley's application of perception-action processes to simulation, we have also found almost complete overlap in the neural substrates associated with imagining a personal past emotional experience and “trying on” the experience of another subject; however, we also found differences in self and other processes, which would not be predicted by the SCM, but are explicit in the PAM (Preston et al. Reference Preston, Bechara, Damasio, Grabowski, Stansfield, Mehta and Damasio2007). In this study, the overall level of brain activation and autonomic arousal were much higher in the self-condition than the other-condition, and subjects recruited additional regions of visual association cortex when imagining another's scenario. These data suggest that online simulation of actual, personal events can differ in both quality and quantity from that of hypothetical events. Importantly, however, we found these differences between self and other only when subjects could not relate well to the situation of the other; there were no differences in neural patterns or autonomic arousal when subjects selected scenarios to which they could relate strongly (Preston et al. Reference Preston, Bechara, Damasio, Grabowski, Stansfield, Mehta and Damasio2007).
This latter interaction reflects an important and overlooked point about the processing of other's actions and states: Perception-action mechanisms require that the subject have an existing representation for the action or state of the other. Thus, monkeys do not have mirror neurons for hand manipulations they do not understand, babies do not imitate gestures that they cannot make, and people cannot resonate with an unfamiliar emotional state and cannot predict your response to a truly novel situation.
We have striking pilot data to support this emphasis on personal representations, as individuals with depression perceive and respond to the distress of others differently than their non-depressed counterparts – they are less personally distressed by the sadness and hopelessness of hospital patients, and they are more likely to feel empathy and offer help to patients with particularly high need (Preston et al., in preparation a).
In another behavioral study, we have found that the mere perception of an emotional facial expression not only activates mirroring in a subject's facial muscles (cf. Dimberg & Oehman Reference Dimberg and Oehman1996), and primes the same valence in the subject (cf. Murphy & Zajonc Reference Murphy and Zajonc1993), but also rapidly activates the semantic-level representation for the specific emotion (e.g., “fear”) (Preston & Stansfield, in press) – this finding is not predicted by models that exclusively rely on motor-based, facial feedback, or mirroring of emotion processing, but it is obvious from basic facts about how information is processed from perception to concept retrieval.
It is exciting and promising to have many researchers agreeing on some basic tenants about how behavior is instantiated – however, as with all complex problems, the devil is in the details. In order to make additional headway from here on out, we must look to the data.
ACKNOWLEDGMENTS
I am indebted to Frans de Waal for encouraging this piece and to R. Brent Stansfield for his feedback and support while writing it.