The acting brain: reviewing the neuroscientific
Istituto di Fisiologia Umana - Università di Parma
During the last years of this ending century we have seen in both neuroscience and philosophy the development of an increasing sense of dissatisfaction for the computational, symbolic account of the brain/mind heralded by functionalism. This, which I suspect is going to lead to a dramatic paradigm-shift for the study of the brain/mind in the next century, is the logical consequence of the intrinsic aporias of a rigid and detached-from-nature version of physical monism. Such post-dualistic account of the brain/mind, when dealing with the "res cogitans" only equipped with the conceptual tools derived from the knowledge of a devitalized, mechanistic "res extensa", is forced either to become anomalous, a "politically correct" form of dualism, or to deny facticity to the phenomenological world. Self-consciousness and intentionality, which, rightly or wrongly as it may be, are considered among the most distinctive features of our species, become paradoxically problematic if to be explained within the logic of functionalism.
In The Paradox of Self-Consciousness Bermúdez provides an exciting and insightful account of how to reconcile physicalism with a biologically plausible description of self-consciousness. The starting point is in my view the decisive one: Bermúdez correctly points out that the supposed intrinsic interdependence between self-consciousness and linguistic self-reference is the source of all types of circularities leading to what he calls the "paradox of self-consciousness". While totally agreeing with Bermúdez, I would add that this is only one particular aspect of the much more pervasive idea that the only possible account of mentality must be the linguistic one. The alternative view proposed by Bermúdez is that of looking for pre-conceptual forms of content in the domains of visual perception, somatic proprioception, spatial perspectivity, and interpersonal relations. Self-consciousness is de-constructed into different sub-components each of which constitutes at the same time a possible evolutionary step towards the accomplishment of a full-fledged, typically human, self-consciousness.
Bermúdez's account is most welcome from a neuroscientific perspective because it is strikingly consonant to many recent empirical findings showing the tight connection that relates the "body in action" with the cognitive aspects of behavior. I will present here some of this evidence, with particular relevance given to some of the features that according to Bermúdez are pertinent to pre-conceptual types of self-consciousness: the self/object dialectic of action, intersubjectivity and the spatial domain.
Some recent results of neurophysiological research clearly provide strong empirical evidence in favor of the existence of multiple neural "representations" of given types of "knowledge" like actions or objects. Far from supporting the view of a highly redundant system, this evidence points to the existence of distinct and specialized neural circuits whose "representational rules" vary along two main dimensions: the frame of reference (egocentric, allocentric) and the degree of specificity (or, conversely, the degree of generalization). Multimodal cortices such as area VIP and sectors of area PF in the posterior parietal cortex, and area F4 in the ventral premotor cortex, code the presence of objects within a limited space sector, peri-personal space (Gentilucci et al. 1988; Graziano et al. 1994; Fogassi et al. 1996; Rizzolatti et al. 1997; Graziano and Gross 1998; Duhamel et al. 1998). Peri-personal space is by definition a motor space, its outer limits being defined by the working space of the different body effectors. This spatial coding relies on an egocentric, often body parts-centered, frame of reference. What is relevant in the spatial coding implemented within these brain sectors is the location, with respect to the living body containing those same brain sectors, of "something" that will become the target of a purposeful action. The quality of that "something" is far less relevant. Indeed the majority of space-selective neurons within the aforementioned areas are not sensitive to the stimuli qualitative features, such as shape or size.
Quite the opposite is what emerges from the study of the neural properties within different cortical regions such as the parietal area AIP and the rostral sector1 of the premotor area F5. They are both characterized by the presence of visuo-motor neurons coding the 3D intrinsic features of objects and the motor schemas suitable to successfully and congruently interact with the same objects by means of goal-related actions (Rizzolatti et al. 1988; Jeannerod et al. 1995; Murata et al. 1997; Sakata and Taira 1994; Murata et al. 1996) The quality of the object in term of shape, size and axis orientation is the relevant feature here. Characteristically, in both AIP and F5 neurons the spatial location is much less important than the physical quality of the object in driving the neural response. The object is the anchor of the reference frame. But this object-centered reference frame, although not related to the object's position with respect to the agent, is nevertheless strongly dependent on the relation with the agent, being the object the target of the agent's action. In premotor area F5 this means that object-centredness does not preclude a relational, if not intentional, representational rule. The object becomes represented as an intentional motor schema.
These brief considerations suggest that one should be cautious when proposing rigid dycothomies between viewer-centered and object-centered reference frames (see also Gallese et al. 1999). This rigid dycothomy in my opinion is the result of the still widespread tendency to consider perception and action as separate domains.
With respect to this latter issue I am not sure that the notion of "affordance" provided by Gibson and used by Bermúdez to make his point captures completely the role of action in determining the content of perception. It is true that according to ecological theories of perception the relation between perception and action is non linear, however, the role assigned by Gibson to action is merely instrumental. Active, but also passive movements, according to Gibson, represent just a tool to capture the high-order invariant features, which are prespecified in the afferent stimulation.
My point is that it is only active movement, which enable us to create representational contents. Thus, I find motor theories of perception more plausible, and perhaps more importantly, more adequate in explaining the empirical evidence provided by neuroscience.
A third different picture emerges from the study of the anterior sector of the STS region and the posterior sector of area F51, two cortical regions that may be highly relevant for social cognition. In these brain regions neurons respond to the observation of specific meaningful actions. In other words they are able to extract the purpose/meaning of the observed action generalizing across different instances of it, such as the quality of the object target of the action, or the quality of the effector performing the action (Gallese et al. 1996; Rizzolatti et al. 1996; Gallese and Goldman 1998; Perrett 1989, 1990). The spatial location of the observed action with respect to the observer can influence the response of only a limited number of these neurons.
In sum, what emerges is the essential relational nature of the motor system. This relational attitude is used also to give, at a pre-conceptual level, (well before the development of linguistic competence), preliminary "intentional" coherence to the array of visual stimuli we are exposed to. An object, as coded by F5 premotor canonical neurons (see Rizzolatti and Gallese 1997; Murata et al. 1997), is transformed from a physical textured pattern of given shape, size and color into something that acquires its meaning in virtue of being constituted as the target of an action. The physical object becomes an "intentional object". At this stage, the nervous system elaborates a code that "classifies" the objects of the external world according to their relational value for the acting subject. The object ceases to exist by itself but acquires a meaning in virtue of its relation to the acting subject.
The same relational attitude is applied when observing other behaving individuals. The observer begins to "understand" the observed behavior of a second party when this process of "motor equivalence" between action observation/execution is set by means of a shared motor representation. F5 mirror neurons are the neural correlate of this shared representation (see Gallese et al. 1996; Rizzolatti et al. 1996; Gallese and Goldman 1998).
I posited (see Gallese 2000) that this notion of motor representation may constitute a pre-conceptual level of analysis of information. From this perspective, agency may represent the key for understanding, both in phylogenetic and ontogenetic terms, how our knowledge of the world is built.
It is clear from this brief and incomplete survey of the neurophysiological literature, that these apparently conflicting representational rules need to be reconciled, were they supposed to provide an ubi consistam to the notion of consciousness. In a broad sense (see also Gallese 1999) the possibility of being conscious depends on the acquired capacity 1) to recognize the existence of multiple frames of reference and 2) to put them in dynamic relation to each other by a continuous process of analogy and differentiation. This capacity likely developed as the best adaptive solution to the powerful pressure exerted by the presence of multiple and, in principle, conflicting frames of reference. Consciousness can be seen as the adaptive tool able to give coherence to these interacting levels of representation. The adaptive logic of consciousness, once rooted into this evolutionary perspective, can be traced back to more ancient mechanisms of which it may represent the human homologue
Is it possible to define the constituent parts of consciousness in terms of the functional properties of a series of neural circuits? The experimental results acquired during the last two decades (see Jeannerod, 1994; 1997), and in particular the results of single neuron recording studies in non-human primates, have demonstrated the essentially relational nature of the motor system, not only from the -obvious- executive point of view, but also in terms of its representational capacities. As I said before, these results point to a central role played by agency in constituting the model of both the self and of the "world outside". The puzzling identity between the phenomenological experience of being the subject of the process of representing oneself as an object and the phenomenological experience of oneself as the object of a third party's representation, may find in this dual aspect of action execution/representation a, still hypothetical, neurobiological explanation.
If consciousness is a model of the world it must incorporate also the notion of the possibility to demarcate the world as that something that sets the limits of the self. In this perspective self and world depend on each others' definition, being different and at the same time intrinsically necessary to each other. Thus, I think that Bermúdez is perfectly right when defining self-consciousness as a "contrastive notion".
As discussed by Bermúdez a nonconceptual point of view is crucial for anchoring the self with respect to the world. A similar concept has been proposed by Metzinger (1999; 2000) when, within his theory of the self-model, he speaks of perspectivalness. According to Metzinger perspectivalness anchors the viewpoint from which "the world outside" is experienced to a temporally extended, non-conceptual first person perspective. But our body is made of different parts, and indeed, as mentioned above, the different parts of the body (e.g., the eyes, the head, the hands) rely on different frames of spatial reference that are "implemented" in specific, distinct and different neural circuits. Furthermore, it is well known that hemispatial neglect, a disturbance of spatial awareness often resulting from lesions of the right posterior parietal cortex, can be exclusively confined either to the peripersonal or to the extrapersonal space.
These results tell us that even one of the single features composing the self construct can be further decomposed, at the neuronal as well as at the neuropsychological level. After reaching these conclusions we desperately need a "glue" capable to give coherence to the cubist multiplicity of perspectives and levels of descriptions produced by this de-constructivist account of the self and its features. My suggestion is that a good candidate for gluing the pieces together might be the motor system, in its double aspect of action generation and action representation.
<1> Area F5 represents the rostralmost sector of the ventral premotor cortex of the macaque brain. F5 can be functionally segregated in at least two sectors: 1) A rostral sector, buried within the posterior bank of the inferior arcuate sulcus, characterized by the presence of "canonical neurons", motorically activated by goal-directed hand and mouth actions, and visually driven by objects whose intrinsic qualities are very often highly correlated with the motor properties coded by the same neuron; 2) A caudal sector, constituted by the cortical convexity part of F5, characterized by the presence of "mirror neurons". Mirror neurons share the motor properties with canonical neurons, from which they differ for their visual properties. Mirror neurons are not driven by object observation: they are driven by the observation of hand or mouth actions, performed by other individuals, that are congruent with the motorically coded ones.
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